<?xml version="1.0" encoding="UTF-8" standalone="no"?>
<!DOCTYPE article PUBLIC "-//NLM//DTD Journal Publishing DTD v2.3 20070202//EN" "journalpublishing.dtd">
<article xmlns:mml="http://www.w3.org/1998/Math/MathML" xmlns:xlink="http://www.w3.org/1999/xlink" article-type="research-article">
<front>
<journal-meta>
<journal-id journal-id-type="publisher-id">Front. Ecol. Evol.</journal-id>
<journal-title>Frontiers in Ecology and Evolution</journal-title>
<abbrev-journal-title abbrev-type="pubmed">Front. Ecol. Evol.</abbrev-journal-title>
<issn pub-type="epub">2296-701X</issn>
<publisher>
<publisher-name>Frontiers Media S.A.</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="doi">10.3389/fevo.2015.00052</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Genetics</subject>
<subj-group>
<subject>Hypothesis and Theory</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Stability and the competition-dispersal trade-off as drivers of speciation and biodiversity gradients</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author" corresp="yes">
<name><surname>Pellissier</surname> <given-names>Lo&#x000EF;c</given-names></name>
<xref ref-type="aff" rid="aff1"><sup>1</sup></xref>
<xref ref-type="aff" rid="aff2"><sup>2</sup></xref>
<xref ref-type="aff" rid="aff3"><sup>3</sup></xref>
<xref ref-type="author-notes" rid="fn001"><sup>&#x0002A;</sup></xref>
<uri xlink:href="http://community.frontiersin.org/people/u/77140"/>
</contrib>
</contrib-group>
<aff id="aff1"><sup>1</sup><institution>Department of Biology, University of Fribourg</institution> <country>Fribourg, Switzerland</country></aff>
<aff id="aff2"><sup>2</sup><institution>Landscape Ecology, Institute of Terrestrial Ecosystems, ETH Z&#x000FC;rich</institution> <country>Z&#x000FC;rich, Switzerland</country></aff>
<aff id="aff3"><sup>3</sup><institution>Swiss Federal Institute for Forest, Snow and Landscape Research</institution> <country>Birmensdorf, Switzerland</country></aff>
<author-notes>
<fn fn-type="edited-by"><p>Edited by: Hao Zhu, Southern Medical University, China</p></fn>
<fn fn-type="edited-by"><p>Reviewed by: Miguel Arenas, Consejo Superior de Investigaciones Cient&#x000ED;ficas, Spain; Nusha Keyghobadi, Western University, Canada</p></fn>
<fn fn-type="corresp" id="fn001"><p>&#x0002A;Correspondence: Lo&#x000EF;c Pellissier, Department of Biology, University of Fribourg, Chemin du Mus&#x000E9;e 10, 1700 Fribourg, Switzerland <email>loic.pellissier&#x00040;unifr.ch</email></p></fn>
<fn fn-type="other" id="fn002"><p>This article was submitted to Evolutionary and Population Genetics, a section of the journal Frontiers in Ecology and Evolution</p></fn>
</author-notes>
<pub-date pub-type="epub">
<day>03</day>
<month>06</month>
<year>2015</year>
</pub-date>
<pub-date pub-type="collection">
<year>2015</year>
</pub-date>
<volume>3</volume>
<elocation-id>52</elocation-id>
<history>
<date date-type="received">
<day>22</day>
<month>03</month>
<year>2015</year>
</date>
<date date-type="accepted">
<day>05</day>
<month>05</month>
<year>2015</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright &#x000A9; 2015 Pellissier.</copyright-statement>
<copyright-year>2015</copyright-year>
<license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/4.0/"><p>This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.</p>
</license>
</permissions>
<abstract><p>The geography of speciation is one of the most contentious topics at the frontier between ecology and evolution. Here, building on previous hypotheses, I propose that ecological constraints on species co-existence mediate the likelihood of speciation, via a trade-off between competitive and dispersal abilities. Habitat stability, as found in the tropics, selects for the evolution of stronger competitive abilities. Since resource investment in competitive and dispersal abilities should trade off, high competition in stable habitats reduces species dispersal ability, decreasing effective population sizes. In smaller local populations, higher fixation rates of molecular substitutions increases the likelihood of speciation. Species diversity triggers more speciation by further increasing the spatial structuring of populations and decreasing effective population sizes. Resource specialization also trades-off with dispersal ability and could account for speciation at higher trophic levels. Biotic interactions may promote parapatric speciation and generate spatial patterns in diversity such as the latitudinal diversity gradient. I discuss evidence for this mechanism and emphasize the need for studies coupling ecology and speciation theory within landscapes across latitude.</p></abstract>
<kwd-group>
<kwd>molecular evolution</kwd>
<kwd>latitude diversity gradient</kwd>
<kwd>biotic interactions</kwd>
<kwd>competition</kwd>
<kwd>dispersal</kwd>
<kwd>population size</kwd>
</kwd-group>
<counts>
<fig-count count="2"/>
<table-count count="1"/>
<equation-count count="5"/>
<ref-count count="120"/>
<page-count count="10"/>
<word-count count="7821"/>
</counts>
</article-meta>
</front>
<body>
<sec sec-type="introduction" id="s1">
<title>Introduction</title>
<p>The extraordinary diversity of species on earth provides infinite motivation to unravel the underlying ecological and evolutionary rules. Evidences that biodiversity is linked to spatial features suggest that speciation mechanisms cannot be understood outside of their geographical context (Levin, <xref ref-type="bibr" rid="B71">1993</xref>). The most famous example of spatial gradient in species diversity is the latitudinal biodiversity gradient that already puzzled Darwin (<xref ref-type="bibr" rid="B20">1859</xref>) and Wallace (<xref ref-type="bibr" rid="B111">1878</xref>). The current global distribution of biodiversity follows a strongly negative gradient from the tropics to the poles across multiple taxonomic groups (Mittelbach et al., <xref ref-type="bibr" rid="B83">2007</xref>). The association between species spatial distribution and diversification is also reflected in the fossil record, where geographic range size is negatively related to speciation (Jablonski and Roy, <xref ref-type="bibr" rid="B58">2003</xref>) and extinction rates (Jablonski, <xref ref-type="bibr" rid="B56">2007</xref>). Classic examples of exceptional events of speciation, including Darwin&#x00027;s finches (Grant and Grant, <xref ref-type="bibr" rid="B46">2011</xref>), <italic>Anolis</italic> lizards (Losos, <xref ref-type="bibr" rid="B74">1998</xref>) or African cichlids (Schliewen et al., <xref ref-type="bibr" rid="B100">1994</xref>; Barluenga et al., <xref ref-type="bibr" rid="B7">2006</xref>), took place in confined spatial areas such as islands or lakes. Together, this suggests that the rate of species diversification is strongly linked to the spatial distribution and connectivity of meta-populations. However, the role played by this aspect of the speciation process in shaping diversity patterns has generally been neglected (Kisel and Barraclough, <xref ref-type="bibr" rid="B63">2010</xref>).</p>
<p>Gavrilets (<xref ref-type="bibr" rid="B39">2014</xref>) highlighted the need to integrate models of community ecology with those developed in speciation theory in order to better understand the processes of speciation. Community ecology and speciation biology share the common interest of understanding what generates clines in species diversity and many theoretical similarities exists between the fields (e.g., the neutral biodiversity theory, Hubbell, <xref ref-type="bibr" rid="B55">2001</xref>). In particular, the link between the latitudinal diversity gradient, the diversity of biotic interactions and the likelihood of speciation is a long-standing idea (Dobzhansky, <xref ref-type="bibr" rid="B21">1950</xref>; MacArthur, <xref ref-type="bibr" rid="B76">1969</xref>). Dobzhansky proposed that predictable tropical climate should select for greater specialization and species diversity. Since differences in either the intensity of speciation or extinction could ultimately account for the latitudinal cline in biodiversity (Weir and Schluter, <xref ref-type="bibr" rid="B113">2007</xref>), a higher frequency of divergent selection along ecological axes in the tropics (Mittelbach et al., <xref ref-type="bibr" rid="B83">2007</xref>), was proposed to trigger frequent events of ecological speciation (Schluter, <xref ref-type="bibr" rid="B102">2009</xref>). Nevertheless, for speciation to occur, a geographically defined group of individuals must diverge from others and accumulate genetic and/or phenotypic differences that distinguish it as a new species (Levin, <xref ref-type="bibr" rid="B71">1993</xref>).</p>
<p>In contrast to the view that speciation is the direct outcome of competition for resources, a trade-off between dispersal and competition/specialization may enhance speciation by affecting effective population size. Fedorov (<xref ref-type="bibr" rid="B33">1966</xref>) remarked that tropical forests are shaped by a multitude of contiguous populations of closely related species and postulated that the role of genetic drift prevails over that of natural selection in shaping new species. Here, building on Fedorov&#x00027;s observations, I propose the hypothesis of a possible direct link between biotic interactions, connectivity among populations, and speciation that may ultimately explain the higher diversity in the tropics (Mittelbach et al., <xref ref-type="bibr" rid="B83">2007</xref>). I argue that under stable conditions, biotic interactions promote speciation via a trade-off between investments in competitive efficiency and dispersal abilities. While the metabolic theory of molecular evolution, which postulates a link between temperature-dependant metabolic rate and speciation, has received recent attention (Allen et al., <xref ref-type="bibr" rid="B1">2006</xref>; Gillooly and Allen, <xref ref-type="bibr" rid="B44">2007</xref>; Stegen et al., <xref ref-type="bibr" rid="B104">2009</xref>; Dowle et al., <xref ref-type="bibr" rid="B22">2013</xref>), the role of neutral parapatric speciation due to lower dispersal in the tropics has remained little explored. Five decades after the publication of Federov&#x00027;s observations and based on new molecular evidences (e.g., Lasso et al., <xref ref-type="bibr" rid="B69">2011</xref>), I hypothesize that the ecological trade-off between resource use efficiency and dispersal abilities promotes higher speciation rates in the tropics.</p>
</sec>
<sec>
<title>Stability selects for high competitive and low dispersal abilities</title>
<p>Brown and Gibson (<xref ref-type="bibr" rid="B13">1983</xref>) rightly stated that &#x0201C;ultimately, all general patterns of diversity must be attributed to physical causes, either historical perturbations or contemporary variation in the physical environment.&#x0201D; In particular, the shaping of species lineages should be linked to the long-term physical history of habitats (Pellissier et al., <xref ref-type="bibr" rid="B89">2014</xref>). Greater stability over geological time periods has long been proposed to promote biodiversity, mostly because the risk of extinction diminishes (Darwin, <xref ref-type="bibr" rid="B20">1859</xref>; Wallace, <xref ref-type="bibr" rid="B111">1878</xref>). Reconstructions of ancient climate indeed indicate that the tropics remained climatically more stable than higher latitudes, and thus should have retained the most ancient lineages (Dynesius and Jansson, <xref ref-type="bibr" rid="B25">2000</xref>). Accordingly, most extant clades have tropical origins, where basal clades in phylogenies are distributed at lower latitudes (Wiens and Donoghue, <xref ref-type="bibr" rid="B115">2004</xref>). While stability obviously prevents species extinction, evidences indicate that speciation is also faster in the tropics (Weir and Schluter, <xref ref-type="bibr" rid="B113">2007</xref>), but the mechanism is poorly described. A self-sustaining mechanism should provide an explanation for the origin of species diversity in stable habitats.</p>
<p>In ecology, stable habitats are traditionally associated with species possessing a particular life history (MacArthur and Wilson, <xref ref-type="bibr" rid="B77">1967</xref>; Grime, <xref ref-type="bibr" rid="B47">1977</xref>). In Grime&#x00027;s <italic>C-S-R</italic> triangle theory, stable habitats support <italic>C</italic> species, which optimize competitive abilities (Grime, <xref ref-type="bibr" rid="B47">1977</xref>). Vegetation climax after ecological successions provide the best examples for the link between increasing stability and competition (Horn, <xref ref-type="bibr" rid="B53">1974</xref>). As vegetation becomes well established in response to persistent climatic conditions, species compete for space, light and nutrients and only those that are most efficient can persist (Horn, <xref ref-type="bibr" rid="B53">1974</xref>; Tilman, <xref ref-type="bibr" rid="B109">1985</xref>). Stable habitats have also been associated with <italic>K</italic> species along the <italic>r-K</italic> gradient of MacArthur and Wilson (<xref ref-type="bibr" rid="B77">1967</xref>). In a stable environment, species densities are close to the carrying capacity (<italic>K</italic>) and species invest more in fewer offspring, increasing the probability of survival to a long adulthood (MacArthur and Wilson, <xref ref-type="bibr" rid="B77">1967</xref>). Ecological successions have counterparts at an evolutionary scale. Examples of &#x0201C;evolutionary successions&#x0201D; have been described in island systems (B&#x000F6;hle et al., <xref ref-type="bibr" rid="B9">1996</xref>; Panero et al., <xref ref-type="bibr" rid="B88">1999</xref>). Darwin (<xref ref-type="bibr" rid="B20">1859</xref>) noted that most tree species make poor long-distance dispersers due to the large size of their seeds and, as a result, new islands are more often colonized by herbaceous species rather than trees. Under competition for resources, herbaceous clades colonizing islands rapidly evolve more competitive traits such as woodiness and tree-like morphologies (B&#x000F6;hle et al., <xref ref-type="bibr" rid="B9">1996</xref>; Panero et al., <xref ref-type="bibr" rid="B88">1999</xref>). Stable environments are associated with species evolutionary trajectory toward higher level of competitive abilities.</p>
<p>Competitive abilities generally trade-off with dispersal abilities, referring to either dispersal distance or dispersal frequency (McPeek and Holt, <xref ref-type="bibr" rid="B81">1992</xref>; Ehrl&#x000E9;n and Groenendael, <xref ref-type="bibr" rid="B27">1998</xref>; Turnbull et al., <xref ref-type="bibr" rid="B110">1999</xref>; Cadotte et al., <xref ref-type="bibr" rid="B16">2006</xref>). In general, plant species that are better competitors do not exhibit adaptations for long distance dispersal (Ehrl&#x000E9;n and Groenendael, <xref ref-type="bibr" rid="B27">1998</xref>). Accordingly, in habitats with stronger competition for light, species with poor dispersal capacities are more prevalent (Ozinga et al., <xref ref-type="bibr" rid="B87">2004</xref>). The evolution of competitive traits over dispersal abilities under varying degrees of stability can be illustrated by simple metapopulation models adapted from Levins and Culver (<xref ref-type="bibr" rid="B72">1971</xref>). Given competition between two species where species 1 is a superior competitor to species 2 defined by the following equations,
<disp-formula id="E1"><mml:math id="M1"><mml:mrow><mml:mtable columnalign='left'><mml:mtr columnalign='left'><mml:mtd columnalign='left'><mml:mrow><mml:mfrac><mml:mrow><mml:mi>d</mml:mi><mml:msub><mml:mi>p</mml:mi><mml:mn>1</mml:mn></mml:msub></mml:mrow><mml:mrow><mml:mi>d</mml:mi><mml:mi>t</mml:mi></mml:mrow></mml:mfrac><mml:mo>=</mml:mo><mml:msub><mml:mi>d</mml:mi><mml:mn>1</mml:mn></mml:msub><mml:msub><mml:mi>p</mml:mi><mml:mn>1</mml:mn></mml:msub><mml:mrow><mml:mo>(</mml:mo><mml:mrow><mml:mn>1</mml:mn><mml:mo>&#x02212;</mml:mo><mml:msub><mml:mi>p</mml:mi><mml:mn>1</mml:mn></mml:msub></mml:mrow><mml:mo>)</mml:mo></mml:mrow><mml:mo>&#x02212;</mml:mo><mml:mi>e</mml:mi><mml:msub><mml:mi>p</mml:mi><mml:mn>1</mml:mn></mml:msub></mml:mrow></mml:mtd></mml:mtr><mml:mtr columnalign='left'><mml:mtd columnalign='left'><mml:mrow><mml:mfrac><mml:mrow><mml:mi>d</mml:mi><mml:msub><mml:mi>p</mml:mi><mml:mn>2</mml:mn></mml:msub></mml:mrow><mml:mrow><mml:mi>d</mml:mi><mml:mi>t</mml:mi></mml:mrow></mml:mfrac><mml:mo>=</mml:mo><mml:msub><mml:mi>d</mml:mi><mml:mn>2</mml:mn></mml:msub><mml:msub><mml:mi>p</mml:mi><mml:mn>2</mml:mn></mml:msub><mml:mrow><mml:mo>(</mml:mo><mml:mrow><mml:mn>1</mml:mn><mml:mo>&#x02212;</mml:mo><mml:msub><mml:mi>p</mml:mi><mml:mn>2</mml:mn></mml:msub><mml:mo>&#x02212;</mml:mo><mml:msub><mml:mi>p</mml:mi><mml:mn>1</mml:mn></mml:msub></mml:mrow><mml:mo>)</mml:mo></mml:mrow><mml:mo>&#x02212;</mml:mo><mml:mi>e</mml:mi><mml:msub><mml:mi>p</mml:mi><mml:mn>2</mml:mn></mml:msub></mml:mrow></mml:mtd></mml:mtr></mml:mtable></mml:mrow></mml:math></disp-formula>
where <italic>p</italic> is the proportion of occupied sites, <italic>d</italic> the dispersal ability to reach unoccupied sites, and <italic>e</italic> an external factor of extinction, which is inversely proportional to environmental stability. The globally stable equilibrium point is given by:
<disp-formula id="E2"><mml:math id="M2"><mml:mrow><mml:mtable columnalign='left'><mml:mtr columnalign='left'><mml:mtd columnalign='left'><mml:mrow><mml:msub><mml:mi>p</mml:mi><mml:mn>1</mml:mn></mml:msub><mml:msup><mml:mrow></mml:mrow><mml:mo>&#x02217;</mml:mo></mml:msup><mml:mo>=</mml:mo><mml:mn>1</mml:mn><mml:mo>&#x02212;</mml:mo><mml:mi>e</mml:mi><mml:mo>/</mml:mo><mml:msub><mml:mi>d</mml:mi><mml:mn>1</mml:mn></mml:msub></mml:mrow></mml:mtd></mml:mtr><mml:mtr columnalign='left'><mml:mtd columnalign='left'><mml:mrow><mml:msub><mml:mi>p</mml:mi><mml:mn>2</mml:mn></mml:msub><mml:msup><mml:mrow></mml:mrow><mml:mo>&#x02217;</mml:mo></mml:msup><mml:mo>=</mml:mo><mml:mn>1</mml:mn><mml:mo>&#x02212;</mml:mo><mml:msub><mml:mi>p</mml:mi><mml:mn>1</mml:mn></mml:msub><mml:mo>&#x02212;</mml:mo><mml:mi>e</mml:mi><mml:mo>/</mml:mo><mml:msub><mml:mi>d</mml:mi><mml:mn>2</mml:mn></mml:msub></mml:mrow></mml:mtd></mml:mtr></mml:mtable></mml:mrow></mml:math></disp-formula></p>
<p>The relative proportion of sites occupied by each species depends on the degree of perturbation relative to the species dispersal ability. In conditions of intermediate stability, both species survive if <italic>d</italic><sub>2</sub> &#x0003E; <italic>d</italic><sub>1</sub>. Ecologically, intermediate level of perturbation maintains the highest level of diversity (Roxburgh et al., <xref ref-type="bibr" rid="B97">2004</xref>). In contrast, stability is expected to promote the dominance of the most competitive species, so that without perturbation (<italic>e</italic> &#x0003D; 0), only the most competitive species <italic>p</italic><sub>1</sub>survives. Therefore, in stable conditions, only the best competitors are expected to co-exist. While a strategy based on dispersal is disadvantaged, stability selects for the evolution of competitive abilities (Calcagno et al., <xref ref-type="bibr" rid="B17">2006</xref>).</p>
<p>Lower dispersal abilities impact the gene flow among individuals in a landscape. Wright (<xref ref-type="bibr" rid="B118">1946</xref>) pointed out the link between limited dispersal and reduced effective population size (<italic>Ne</italic>): &#x0201C;It is shown that in the absence of disturbing factors, short range dispersal [&#x02026;] leads to considerable differentiation not only among small subdivisions but also of large ones.&#x0201D; Limited dispersal leads to a less connected network of gene flow between populations and thus causes a decrease in effective population size. According to Wright&#x00027;s model with limited dispersal, isolation-by-distance reduces effective population size, even for species that are spread across a wide landscape. The resulting neighborhood effective population size is lower than the census size and related to species dispersal abilities by the following equation:
<disp-formula id="E3"><mml:math id="M3"><mml:mrow><mml:mi>N</mml:mi><mml:mi>e</mml:mi><mml:mo>=</mml:mo><mml:mn>4</mml:mn><mml:mi>&#x003C0;</mml:mi><mml:msub><mml:mi>&#x003C3;</mml:mi><mml:mi>d</mml:mi></mml:msub><mml:msup><mml:mrow></mml:mrow><mml:mn>2</mml:mn></mml:msup><mml:mi>D</mml:mi></mml:mrow></mml:math></disp-formula>
where <italic>D</italic> is the density of pairs contributing to the reproduction and &#x003C3;<sub><italic>d</italic></sub> the standard deviation of dispersal distance representing the dispersal kernel (Wright, <xref ref-type="bibr" rid="B118">1946</xref>). This model linking effective population size and dispersal is in line with the positive correlation between the observed range sizes of species and their dispersal abilities (Gaston, <xref ref-type="bibr" rid="B36">1998</xref>). Together, ecological and evolutionary demographic theories suggest a direct connection between stability, competition, lower dispersal, and decreased effective population size (Figure <xref ref-type="fig" rid="F1">1</xref>).</p>
<fig id="F1" position="float">
<label>Figure 1</label>
<caption><p><bold>Schematic representation of the mechanism of speciation in a stable habitat</bold>. Habitat stability as found in the tropics selects for the evolution of stronger competitive abilities (<italic>C</italic>). Since resource investment in competition and dispersal (<italic>d</italic>) should trade off, inferior dispersal in competitive species implies a decrease in effective population size (<italic>Ne</italic>). In smaller populations, higher fixation rate of molecular substitutions (&#x003BC;) increases the likelihood of speciation events. Higher diversity further promotes diversity since the presence of more species increases spatial structuring of populations, favoring genetic differentiation, and speciation.</p></caption>
<graphic xlink:href="fevo-03-00052-g0001.tif"/>
</fig>
</sec>
<sec>
<title>Population size, nearly-neutral substitutions and speciation</title>
<p>A decrease in population size causes an increase in the rate of non-neutral substitutions (Ohta, <xref ref-type="bibr" rid="B85">1992</xref>; Lanfear et al., <xref ref-type="bibr" rid="B68">2014</xref>), and also in the rate of neutral substitution under specific geometric (e.g., non-circular meta-population distribution, Allen et al., <xref ref-type="bibr" rid="B2">2015</xref>), or demographic conditions (e.g., overlapping generations, Balloux and Lehmann, <xref ref-type="bibr" rid="B6">2012</xref>). As predicted by the nearly neutral theory of molecular evolution (Ohta, <xref ref-type="bibr" rid="B85">1992</xref>), a decrease in effective population size (<italic>Ne</italic>) leads to easier fixation of nearly-neutral mutations (Ohta, <xref ref-type="bibr" rid="B85">1992</xref>; Lanfear et al., <xref ref-type="bibr" rid="B68">2014</xref>). The probability &#x003BC;<italic>f</italic> that the allele will be fixed in the population was first derived by Kimura (<xref ref-type="bibr" rid="B62">1957</xref>) and depends upon the effective <italic>Ne</italic> and census population sizes <italic>N</italic> and the strength of selection <italic>s</italic> as:
<disp-formula id="E4"><mml:math id="M4"><mml:mrow><mml:mi>&#x003BC;</mml:mi><mml:mi>f</mml:mi><mml:mo>=</mml:mo><mml:mfrac><mml:mrow><mml:mn>2</mml:mn><mml:mi>s</mml:mi><mml:mi>N</mml:mi><mml:mi>e</mml:mi><mml:mo>/</mml:mo><mml:mi>N</mml:mi></mml:mrow><mml:mrow><mml:mn>1</mml:mn><mml:mo>&#x02212;</mml:mo><mml:msup><mml:mi>e</mml:mi><mml:mrow><mml:mo>&#x02212;</mml:mo><mml:mn>4</mml:mn><mml:mi>s</mml:mi><mml:mi>N</mml:mi><mml:mi>e</mml:mi></mml:mrow></mml:msup></mml:mrow></mml:mfrac></mml:mrow></mml:math></disp-formula></p>
<p>In the case of small effective population size, the coefficient of selection <italic>s</italic> is balanced by drift. As the effective population size decreases, the influence of drift increases, resulting in a higher ratio of non-synonymous to synonymous substitutions (<italic>dN/dS</italic>) (Kryazhimskiy and Plotkin, <xref ref-type="bibr" rid="B65">2008</xref>). In particular, the probability of fixation of slightly deleterious mutations increases rapidly and approaches the neutral value (Ohta, <xref ref-type="bibr" rid="B85">1992</xref>). Tachida and Iizuka (<xref ref-type="bibr" rid="B107">1991</xref>) further suggested that smaller population size might also increase the probability of fixation of slightly beneficial mutations, in comparison with the case of extensive dispersal within a large population. Selection can thus be stronger in small than in large populations (Ohta, <xref ref-type="bibr" rid="B85">1992</xref>), but this depends on how the rate of migration scales with population size (Gavrilets and Gibson, <xref ref-type="bibr" rid="B40">2002</xref>). As theoretically expected, accelerated rates of non-synonymous molecular substitution are typically found in geographically restricted populations, such as on islands (Johnson and Seger, <xref ref-type="bibr" rid="B61">2001</xref>; Woolfit and Bromham, <xref ref-type="bibr" rid="B117">2005</xref>).</p>
<p>In stable habitats, species should invest in competitive rather than dispersal traits, and reduced effective population size should increase intra-specific genetic structure (Wright, <xref ref-type="bibr" rid="B118">1946</xref>; Ohta, <xref ref-type="bibr" rid="B85">1992</xref>). The link between dispersal and genetic differentiation among lineages found in coral reef fishes (Riginos et al., <xref ref-type="bibr" rid="B94">2014</xref>) or plants (Hardy et al., <xref ref-type="bibr" rid="B49">2006</xref>; Duminil et al., <xref ref-type="bibr" rid="B24">2007</xref>; Theim et al., <xref ref-type="bibr" rid="B108">2014</xref>) suggests a direct link between dispersal, effective population size, and genetic structure. Furthermore, assuming a trade-off between competitive and dispersal abilities, intra-specific non-synonymous substitutions should correlate with traits representing syndromes of a <italic>K</italic> strategy. Accordingly, plant height showed a positive correlation with the ratio of non-synonymous to synonymous substitutions (<italic>dN/dS</italic>) across 138 families of flowering plants (Lanfear et al., <xref ref-type="bibr" rid="B67">2013</xref>; Bromham et al., <xref ref-type="bibr" rid="B12">2015</xref>), while longevity was a strong predictor of this ratio in animals (Romiguier et al., <xref ref-type="bibr" rid="B96">2014</xref>). Similarly, large mammals and birds have a higher rate of amino acid substitutions in proteins (Popadin et al., <xref ref-type="bibr" rid="B92">2007</xref>; Weber et al., <xref ref-type="bibr" rid="B112">2014</xref>). In mammals, the subdivision of a species into sub-populations, such as in the case of competition for territories, promotes both high rates of speciation and chromosomal evolution consistent with an effect of small population size (Bush et al., <xref ref-type="bibr" rid="B15">1977</xref>). Thus, as expected from a link between competitive abilities and effective population size, species displaying traits related to competition have a greater rate of non-neutral substitutions triggering protein evolution (Popadin et al., <xref ref-type="bibr" rid="B92">2007</xref>; Lanfear et al., <xref ref-type="bibr" rid="B68">2014</xref>; Romiguier et al., <xref ref-type="bibr" rid="B96">2014</xref>; Weber et al., <xref ref-type="bibr" rid="B112">2014</xref>).</p>
<p>Organisms prioritizing competitive over dispersal abilities can become geographically isolated more easily, which should enhance speciation (Mayr, <xref ref-type="bibr" rid="B79">1963</xref>). For marine fishes the association between genetic structure, dispersal and species richness suggests that reduction in gene flow can promote speciation (Riginos et al., <xref ref-type="bibr" rid="B94">2014</xref>). Kisel and Barraclough (<xref ref-type="bibr" rid="B63">2010</xref>) found that both dispersal and gene flow in terrestrial taxa were good predictors of speciation rates. Furthermore, small ranged species are over-represented in global biodiversity, which may indicate that speciation via dispersal limitation and small population size is an important mechanism in nature (Gaston, <xref ref-type="bibr" rid="B36">1998</xref>). Under limited dispersal, speciation may arise from gradual separation of sub-populations as molecular substitutions become fixed locally (Figure <xref ref-type="fig" rid="F1">1</xref>). Prezygotic or postzygotic isolating barriers may further counter gene flow to avoid maladapted hybrids (Mayr, <xref ref-type="bibr" rid="B79">1963</xref>; Ramsey et al., <xref ref-type="bibr" rid="B93">2003</xref>; Lukhtanov et al., <xref ref-type="bibr" rid="B75">2005</xref>; McBride and Singer, <xref ref-type="bibr" rid="B80">2010</xref>). Greater isolation by distance (Martin and McKay, <xref ref-type="bibr" rid="B78">2004</xref>), genetic divergence (Eo et al., <xref ref-type="bibr" rid="B31">2008</xref>), but limited occurrence of hybrids (Hopkins, <xref ref-type="bibr" rid="B52">2013</xref>; Surget-Groba and Kay, <xref ref-type="bibr" rid="B106">2013</xref>) has been documented in the tropics and may represent on-going speciation events within local sub-populations.</p>
<p>Non-synonymous substitutions arising in small populations could promote evolution of novel ecological preferences. Since the rate of fixation of non-neutral mutations might be higher (Tachida and Iizuka, <xref ref-type="bibr" rid="B107">1991</xref>; Ohta, <xref ref-type="bibr" rid="B85">1992</xref>) and proteins evolve faster in small populations (Ohta, <xref ref-type="bibr" rid="B86">2002</xref>), this may increase the overall rate of morphological evolution. For instance, in the fossil record small ranged and transient trilobite fossil species show increased morphological variation (Hopkins, <xref ref-type="bibr" rid="B51">2011</xref>), while large ranged species are more likely to show morphological stasis (Gould and Eldredge, <xref ref-type="bibr" rid="B45">1977</xref>). As formulated in the theory of punctuated equilibria (Gould and Eldredge, <xref ref-type="bibr" rid="B45">1977</xref>; Eldredge et al., <xref ref-type="bibr" rid="B28">2005</xref>), ecological innovations might arise at higher frequency in smaller populations. This would also explain the faster rate of morphological evolution in tropical islands (Millien, <xref ref-type="bibr" rid="B82">2006</xref>) and lakes (Schliewen et al., <xref ref-type="bibr" rid="B100">1994</xref>), where population size is smaller (Woolfit and Bromham, <xref ref-type="bibr" rid="B117">2005</xref>) compared to larger continental or ocean surface. Stable habitats reunite the theoretical conditions expected to fuel speciation, including lower effective population size, local mating linked to dispersal limitation and high levels of local genetic variation (Gavrilets, <xref ref-type="bibr" rid="B38">2004</xref>). Together this suggests that molecular evolution fuelling speciation is faster under stable conditions, high competition and limited dispersal, which is characteristic of the tropics. Population differentiation might be further fuelled by higher metabolic and mutation rates expected at lower latitudes (Wright et al., <xref ref-type="bibr" rid="B119">2006</xref>; Stegen et al., <xref ref-type="bibr" rid="B104">2009</xref>).</p>
<p>The current argument suggests a link between rate of molecular substitution and rate of speciation. Evidences of a link between the rates of molecular evolution and diversification have been reported (Eo and DeWoody, <xref ref-type="bibr" rid="B30">2010</xref>; Lanfear et al., <xref ref-type="bibr" rid="B66">2010</xref>; see Dowle et al., <xref ref-type="bibr" rid="B22">2013</xref>). For instance, Lanfear et al. (<xref ref-type="bibr" rid="B66">2010</xref>) identified a correlation between clade rates of molecular evolution and net-diversification in birds. However, the demonstration that the correlation between molecular evolution and speciation hinges on population sizes would require a sampling at the scale of population subdivision. Moreover, as raised by Dowle et al. (<xref ref-type="bibr" rid="B22">2013</xref>), there is currently a lack of evidence of differential population size along latitudinal gradient. The absence of evidence primarily result the lack of studies investigating the genetic structure of population with a comparable sampling design across latitudes. Nevertheless, many studies highlight unexpected high genetic structure in low latitude species (Martin and McKay, <xref ref-type="bibr" rid="B78">2004</xref>; Born et al., <xref ref-type="bibr" rid="B10">2008</xref>; Eo et al., <xref ref-type="bibr" rid="B31">2008</xref>; Lasso et al., <xref ref-type="bibr" rid="B69">2011</xref>), which provide clues of a lower gene flow and smaller effective population sizes due to limited dispersal. Fedorov&#x00027;s ideas relied on the hypothesis of higher rate self-pollination in tropical trees, which was later contradicted (Bawa, <xref ref-type="bibr" rid="B8">1974</xref>). Gene flow through pollen dispersal in tropical trees could potentially occur across long distances (White et al., <xref ref-type="bibr" rid="B114">2002</xref>), but whether pollen transfer across large distance is common or not still remains to be documented across many species. Further studies are therefore required to quantify gene flow among populations across latitudes.</p>
<p>At the other extreme, in less stable environments larger range size resulting from higher dispersal may buffer species against extinction, as suggested by the positive relationship between range size and duration in the fossil record (Jablonski, <xref ref-type="bibr" rid="B57">2008</xref>). This could explain the larger range size at higher latitudes (Rapoport&#x00027;s rule, Stevens, <xref ref-type="bibr" rid="B105">1989</xref>), which may reduce the risk of extinction under less stable environmental conditions. Species with larger range size have greater dispersal ability (Gaston, <xref ref-type="bibr" rid="B36">1998</xref>) and shorter generation time, like <italic>r</italic> species along the <italic>r-K</italic> gradient (MacArthur and Wilson, <xref ref-type="bibr" rid="B77">1967</xref>). Species with shorter generation time accumulate synonymous substitutions faster and generally show a higher level of neutral polymorphism than species with greater longevity or offspring quality (Lanfear et al., <xref ref-type="bibr" rid="B68">2014</xref>; Romiguier et al., <xref ref-type="bibr" rid="B96">2014</xref>). Species with a wide distribution and high dispersal are stabilized in their genetic variation by their large population size and the process of gene flow (Gould and Eldredge, <xref ref-type="bibr" rid="B45">1977</xref>), but which also limits morphological or ecological evolution. Yet, at higher latitude, in less stable environments, speciation may also happen neutrally related to species range dynamics. For instance, range dynamic in interaction with habitat heterogeneity can result in range fragmentation and high rate of speciation (Arenas et al., <xref ref-type="bibr" rid="B5">2012</xref>, <xref ref-type="bibr" rid="B4">2013</xref>; Mona et al., <xref ref-type="bibr" rid="B84">2014</xref>). Populations in expansion are expected to fix mutations though genetic drift occurring in populations located on the edge of the expansion, which may promote speciation (Excoffier and Ray, <xref ref-type="bibr" rid="B32">2008</xref>). However, pronounced range dynamic at higher latitude should also have increased extinction rates (Dynesius and Jansson, <xref ref-type="bibr" rid="B25">2000</xref>). Better sampled phylogenies at the scale of ongoing population divisions (i.e., infra-species) within landscapes is necessary to compare diversification processes across latitudes.</p>
</sec>
<sec>
<title>Diversity increases landscape fragmentation</title>
<p>Species diversity itself could be a driver of species diversification following the famous &#x0201C;diversity begets diversity&#x0201D; model, since speciation rates correlate with diversity (Emerson and Kolm, <xref ref-type="bibr" rid="B29">2005</xref>). I propose that, when more than one species co-exist in a landscape, and assuming the same potential density of pairs in all species, the effective population size of a species <italic>i</italic> follow the formula:
<disp-formula id="E5"><mml:math id="M5"><mml:mrow><mml:mi>N</mml:mi><mml:mi>e</mml:mi><mml:mo>=</mml:mo><mml:mfrac><mml:mrow><mml:mn>4</mml:mn><mml:mi>&#x003C0;</mml:mi><mml:msubsup><mml:mi>&#x003C3;</mml:mi><mml:mrow><mml:mi>d</mml:mi><mml:mi>i</mml:mi></mml:mrow><mml:mn>2</mml:mn></mml:msubsup><mml:mi>D</mml:mi></mml:mrow><mml:mrow><mml:mi>S</mml:mi><mml:mi>p</mml:mi></mml:mrow></mml:mfrac></mml:mrow></mml:math></disp-formula>
where <italic>D</italic> is the density of pairs contributing to the reproduction &#x003C3;<sub><italic>di</italic></sub> the standard deviation of dispersal distance of the species <italic>i</italic> and <italic>Sp</italic> the number of species. An increase in species diversity causes a decrease in species relative density, thus reducing effective population size. Increasing the number of species thus decreases the local population size, enhancing genetic drift, and the likelihood of divergence (Wright, <xref ref-type="bibr" rid="B118">1946</xref>; Ohta, <xref ref-type="bibr" rid="B85">1992</xref>).</p>
<p>A higher rate of neutral molecular evolution has been found in tropical clades (Wright et al., <xref ref-type="bibr" rid="B119">2006</xref>; Gillman et al., <xref ref-type="bibr" rid="B42">2009</xref>), and in clades with greater numbers of species (Duchene and Bromham, <xref ref-type="bibr" rid="B23">2013</xref>), but small population size was dismissed as an explanation based on the assumption that neutral substitution is not influenced by population size (Charlesworth, <xref ref-type="bibr" rid="B19">2009</xref>). However, the neutral substitution rate is higher for smaller populations in the presence of overlapping generations, as is largely the case in tropical species (Charlesworth, <xref ref-type="bibr" rid="B19">2009</xref>; Balloux and Lehmann, <xref ref-type="bibr" rid="B6">2012</xref>). In addition, limited dispersal in highly diverse landscape may shape more patchy distribution of populations with non-regular spatial structures (Figure <xref ref-type="fig" rid="F1">1</xref>). Allen et al. (<xref ref-type="bibr" rid="B2">2015</xref>) demonstrated that singular geometric spatial structures of individuals or populations that form in high diversity landscapes (Figure <xref ref-type="fig" rid="F1">1</xref>) can increase the rate of synonymous substitution. The higher rate of molecular evolution in tropical clades supports the central role of effective population size in tropical speciation (Wright et al., <xref ref-type="bibr" rid="B119">2006</xref>; Gillman et al., <xref ref-type="bibr" rid="B42">2009</xref>, <xref ref-type="bibr" rid="B43">2012</xref>). Therefore, a higher rate of both neutral and non-neutral substitution could fuel speciation in stable habitats in interaction with population sizes.</p>
</sec>
<sec>
<title>Ecological island syndrome at higher trophic levels</title>
<p>Specialisation of antagonistic and mutualistic interactions is another typical response of higher trophic levels to resource competition in stable habitats (Futuyma and Moreno, <xref ref-type="bibr" rid="B35">1988</xref>). Specialisation allows an increase in the efficiency of the use of a given resource, to the detriment of a wider trophic regime (Futuyma and Moreno, <xref ref-type="bibr" rid="B35">1988</xref>). Trophic specialization is central to models of adaptive radiation (Schluter, <xref ref-type="bibr" rid="B101">2000</xref>), and may underlie much of the shaping of species diversity (Jocque et al., <xref ref-type="bibr" rid="B60">2010</xref>; Forister et al., <xref ref-type="bibr" rid="B34">2012</xref>). Like traits related to competitive abilities, trophic specialization is expected to be negatively related to dispersal, as the probability of finding suitable conditions elsewhere declines with specialization (Salisbury et al., <xref ref-type="bibr" rid="B98">2012</xref>). Following Janzen (<xref ref-type="bibr" rid="B59">1968</xref>), who described plants as islands in space for the herbivorous insects that feed on them, a specialist will only be distributed in the area overlapping host or prey species, thus increasing the fragmentation of its populations (Figure <xref ref-type="fig" rid="F2">2</xref>). Hence, specialization results in a limited population size, which should increase the probability of speciation (Wright, <xref ref-type="bibr" rid="B118">1946</xref>; Ohta, <xref ref-type="bibr" rid="B85">1992</xref>).</p>
<fig id="F2" position="float">
<label>Figure 2</label>
<caption><p><bold>Example of biotic interactions impacting the spatial configuration of populations</bold>. The butterfly <italic>Jalmenus evagoras</italic> of the Lycaenidae feeds on &#x0007E;16 <italic>Acacia</italic> plant species <bold>(A)</bold> (Pierce and Nash, <xref ref-type="bibr" rid="B91">1999</xref>), and is in an obligatory mutualism with principally two <italic>Iridomyrmex</italic> ant species (<italic>Iridomyrmex anceps</italic>, <italic>I. rufoniger</italic>) <bold>(B)</bold>. As a consequence, the distribution of <italic>J. evagoras</italic> <bold>(C)</bold> is not only constrained by the host plant, but also by the mutualist ant, causing population fragmentation and likely genetic differentiation (Eastwood et al., <xref ref-type="bibr" rid="B26">2006</xref>). <bold>(D)</bold> Schematic view of the trophic link between the butterfly <italic>J. evagoras</italic> and its host plants and ant species. Distribution maps were obtained using species distribution models with a random forest statistical approach applied to occurrences from <ext-link ext-link-type="uri" xlink:href="http://www.gbif.org/">http://www.gbif.org/</ext-link>. Pseudo-absences were generated randomly across Australia. The distribution of <italic>J. evagoras</italic> was constrained by the forecasted range of the host plants and mutualistic ant species. Acacia spectabilis image by Melburnian [Own work (digital photograph by author)] [CC BY 3.0 (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/3.0">http://creativecommons.org/licenses/by/3.0</ext-link>)], via Wikimedia Commons. Jalmenus-evagoras-ventral image by Benjamint444 (Own work) [GFDL 1.2 (<ext-link ext-link-type="uri" xlink:href="http://www.gnu.org/licenses/old-licenses/fdl-1.2.html">http://www.gnu.org/licenses/old-licenses/fdl-1.2.html</ext-link>)], via Wikimedia Commons.</p></caption>
<graphic xlink:href="fevo-03-00052-g0002.tif"/>
</fig>
<p>Fragmentation of populations following the appearance of strong biotic interactions may trigger an increased rate of molecular substitution and speciation (Gavrilets et al., <xref ref-type="bibr" rid="B41">2000</xref>). In both marine and terrestrial ecosystems, biotic specialization is associated with marked intra-specific spatial genetic structure. Fishes in close mutualism with corals, sea urchins, or anemones show exceptional spatial genetic structure (Hoffman et al., <xref ref-type="bibr" rid="B50">2005</xref>) and a higher rate of diversification (Litsios et al., <xref ref-type="bibr" rid="B73">2012</xref>). Zayed and Packer (<xref ref-type="bibr" rid="B120">2007</xref>) found that a species of bee with a specialized pollen diet had considerably higher spatial genetic variation among populations compared to a generalist counterpart. Strong spatial genetic differentiation has also been found among populations of mutualistic butterflies of the family Lycaenidae (Eastwood et al., <xref ref-type="bibr" rid="B26">2006</xref>; Pellissier et al., <xref ref-type="bibr" rid="B90">2012</xref>), which has led to even stronger differentiation in one of their specialized parasitoid wasps (Anton et al., <xref ref-type="bibr" rid="B3">2007</xref>). Higher degrees of specialization or multiple biotic constraints (e.g., the required presence of a mutualist in addition to the trophic host, Figure <xref ref-type="fig" rid="F2">2</xref>) should reinforce the degree of fragmentation. The idea that biotic constraints play a major role in the process of tropical diversification is not novel (Dobzhansky, <xref ref-type="bibr" rid="B21">1950</xref>), and has led to the hypothesis that the latitudinal diversity gradient is mainly due to latitudinal differences in biotic interactions (Wallace, <xref ref-type="bibr" rid="B111">1878</xref>; Dobzhansky, <xref ref-type="bibr" rid="B21">1950</xref>). Jocque et al. (<xref ref-type="bibr" rid="B60">2010</xref>) also argued that the trade-off between specialization and dispersal underlies the latitudinal diversity gradient, since specialized biotic interactions are more common in the tropics (Schemske et al., <xref ref-type="bibr" rid="B99">2009</xref>). Accordingly, I propose that speciation associated with biotic interaction may not be necessarily due to filling novel niches, but results from spatial fragmentation of populations due to limited dispersal which promotes local divergence.</p>
</sec>
<sec sec-type="conclusion" id="s2">
<title>Conclusion</title>
<p>Although it is becoming increasingly clear that many tropical clades experience higher speciation rates, very little is known about the processes of divergence among populations (Surget-Groba and Kay, <xref ref-type="bibr" rid="B106">2013</xref>). Increased evidences of unexpected high degree of genetic differentiation among populations of tropical species argue for pursuing Fedorov&#x00027;s idea (Lasso et al., <xref ref-type="bibr" rid="B69">2011</xref>). Here, I discussed how biotic constraints may modulate population size, the rate of molecular evolution and speciation in stable habitats like those found in the tropics. I propose that under stable environmental conditions, biotic constraints promote speciation through a trade-off between competition and dispersal. In turn, this can be extended to specialization-dispersal trade-offs at higher trophic levels (Jocque et al., <xref ref-type="bibr" rid="B60">2010</xref>). The current theory can be broken down into a series of elements which can be validated independently on empirical data and thus represent a testable framework (Table <xref ref-type="table" rid="T1">1</xref>). The strength of the present concept is its ability to bridge theories in ecology (<italic>C-S-R</italic>, <italic>r-K</italic> theories, Rapoport&#x00027;s rule), paleontology (punctuated equilibria) and evolution (the nearly neutral theory of molecular evolution). Only by cutting across disciplines can we hope to unravel the mechanisms driving the origin of species diversity on earth. The continued reductions in DNA sequencing costs which allow sampling many populations across tropical and temperate landscape, and estimating both <italic>Ne</italic> and substitution rates, promise many advances in the years to come.</p>
<table-wrap position="float" id="T1">
<label>Table 1</label>
<caption><p><bold>List of syndromes that provide indication of the links between competitive abilities, dispersal abilities, population sizes, and species diversification along a latitudinal gradient</bold>.</p></caption>
<table frame="hsides" rules="groups">
<thead>
<tr>
<th/>
<th align="center"><bold>Sign</bold></th>
<th align="center" colspan="2"><bold>Syndromes</bold></th>
<th align="left"><bold>References</bold></th>
</tr>
<tr>
<th/>
<th/>
<th align="center"><bold>X</bold></th>
<th align="center"><bold>Y</bold></th>
<th/>
</tr>
</thead>
<tbody>
<tr>
<td align="left" valign="top">Stability and latitude</td>
<td align="center" valign="top">&#x02212;</td>
<td align="left" valign="top">Diversity</td>
<td align="left" valign="top">Latitude</td>
<td align="left" valign="top">Gaston, <xref ref-type="bibr" rid="B37">2000</xref>; Kreft and Jetz, <xref ref-type="bibr" rid="B64">2007</xref>; Rohde, <xref ref-type="bibr" rid="B95">2007</xref></td>
</tr>
<tr>
<td/>
<td align="center" valign="top">&#x02212;</td>
<td align="left" valign="top">Intra-specific genetic structure</td>
<td align="left" valign="top">Latitude</td>
<td align="left" valign="top">Martin and McKay, <xref ref-type="bibr" rid="B78">2004</xref>; Born et al., <xref ref-type="bibr" rid="B10">2008</xref>; Eo et al., <xref ref-type="bibr" rid="B31">2008</xref></td>
</tr>
<tr>
<td/>
<td align="center" valign="top">&#x02212;</td>
<td align="left" valign="top">Rate of molecular evolution</td>
<td align="left" valign="top">Latitude</td>
<td align="left" valign="top">Wright et al., <xref ref-type="bibr" rid="B119">2006</xref>; Gillman et al., <xref ref-type="bibr" rid="B42">2009</xref>;</td>
</tr>
<tr>
<td/>
<td align="center" valign="top">&#x0002B;</td>
<td align="left" valign="top">Range size</td>
<td align="left" valign="top">Latitude</td>
<td align="left" valign="top">Stevens, <xref ref-type="bibr" rid="B105">1989</xref>; Gaston, <xref ref-type="bibr" rid="B36">1998</xref></td>
</tr>
<tr>
<td/>
<td align="center" valign="top">&#x02212;</td>
<td align="left" valign="top">Lineage age</td>
<td align="left" valign="top">Latitude</td>
<td align="left" valign="top">Weir and Schluter, <xref ref-type="bibr" rid="B113">2007</xref></td>
</tr>
<tr>
<td/>
<td align="center" valign="top">&#x02212;</td>
<td align="left" valign="top">Speciation rate</td>
<td align="left" valign="top">Latitude</td>
<td align="left" valign="top">Cardillo, <xref ref-type="bibr" rid="B18">1999</xref>; Weir and Schluter, <xref ref-type="bibr" rid="B113">2007</xref></td>
</tr>
<tr>
<td/>
<td align="center" valign="top">&#x02212;</td>
<td align="left" valign="top">Cryptic diversity</td>
<td align="left" valign="top">Latitude</td>
<td align="left" valign="top">Burns et al., <xref ref-type="bibr" rid="B14">2008</xref>; Smith et al., <xref ref-type="bibr" rid="B103">2008</xref></td>
</tr>
<tr>
<td align="left" valign="top">Stability and competition</td>
<td align="center" valign="top">&#x0002B;</td>
<td align="left" valign="top">Environmental stability</td>
<td align="left" valign="top">More competitive species</td>
<td align="left" valign="top">Horn, <xref ref-type="bibr" rid="B53">1974</xref>; Tilman, <xref ref-type="bibr" rid="B109">1985</xref></td>
</tr>
<tr>
<td align="left" valign="top">Competition and evolution</td>
<td align="center" valign="top">&#x0002B;</td>
<td align="left" valign="top">Longevity</td>
<td align="left" valign="top">Non-synonymous substitution</td>
<td align="left" valign="top">Lanfear et al., <xref ref-type="bibr" rid="B68">2014</xref>; Romiguier et al., <xref ref-type="bibr" rid="B96">2014</xref></td>
</tr>
<tr>
<td/>
<td align="center" valign="top">&#x0002B;</td>
<td align="left" valign="top">Body size</td>
<td align="left" valign="top">Amino-acid substitution</td>
<td align="left" valign="top">Bromham, <xref ref-type="bibr" rid="B11">2002</xref>; Popadin et al., <xref ref-type="bibr" rid="B92">2007</xref>; Weber et al., <xref ref-type="bibr" rid="B112">2014</xref></td>
</tr>
<tr>
<td align="left" valign="top">Dispersal and population size</td>
<td align="center" valign="top">&#x0002B;</td>
<td align="left" valign="top">Dispersal</td>
<td align="left" valign="top">Population size</td>
<td align="left" valign="top">Hubbell, <xref ref-type="bibr" rid="B54">1979</xref></td>
</tr>
<tr>
<td/>
<td align="center" valign="top">&#x02212;</td>
<td align="left" valign="top">Dispersal</td>
<td align="left" valign="top">Intra-specific genetic structure</td>
<td align="left" valign="top">Hardy et al., <xref ref-type="bibr" rid="B49">2006</xref>; Kisel and Barraclough, <xref ref-type="bibr" rid="B63">2010</xref></td>
</tr>
<tr>
<td/>
<td align="center" valign="top">&#x0002B;</td>
<td align="left" valign="top">Dispersal</td>
<td align="left" valign="top">Range size</td>
<td align="left" valign="top">Gaston, <xref ref-type="bibr" rid="B36">1998</xref>; Lester et al., <xref ref-type="bibr" rid="B70">2007</xref></td>
</tr>
<tr>
<td align="left" valign="top">Population size and evolution</td>
<td align="center" valign="top">&#x0002B;</td>
<td align="left" valign="top">Rate of molecular evolution</td>
<td align="left" valign="top">Rate of speciation</td>
<td align="left" valign="top">Wright et al., <xref ref-type="bibr" rid="B119">2006</xref>; Gillman et al., <xref ref-type="bibr" rid="B42">2009</xref>; Lanfear et al., <xref ref-type="bibr" rid="B66">2010</xref>; Gillman et al., <xref ref-type="bibr" rid="B43">2012</xref></td>
</tr>
<tr>
<td/>
<td align="center" valign="top">&#x0002B;</td>
<td align="left" valign="top">Range size</td>
<td align="left" valign="top">Duration in fossil record</td>
<td align="left" valign="top">Jablonski, <xref ref-type="bibr" rid="B57">2008</xref></td>
</tr>
<tr>
<td/>
<td align="center" valign="top">&#x02212;</td>
<td align="left" valign="top">Duration in fossil record</td>
<td align="left" valign="top">Fossil morphological diversity</td>
<td align="left" valign="top">Hopkins, <xref ref-type="bibr" rid="B51">2011</xref></td>
</tr>
<tr>
<td/>
<td align="center" valign="top">&#x02212;</td>
<td align="left" valign="top">Range size</td>
<td align="left" valign="top">Speciation</td>
<td align="left" valign="top">Jablonski and Roy, <xref ref-type="bibr" rid="B58">2003</xref></td>
</tr>
<tr>
<td/>
<td align="center" valign="top">&#x02212;</td>
<td align="left" valign="top">Range size</td>
<td align="left" valign="top">Species diversity</td>
<td align="left" valign="top">Gaston, <xref ref-type="bibr" rid="B36">1998</xref></td>
</tr>
<tr>
<td/>
<td align="center" valign="top">&#x02212;</td>
<td align="left" valign="top">Population size</td>
<td align="left" valign="top">Rate of molecular evolution</td>
<td align="left" valign="top">Ohta, <xref ref-type="bibr" rid="B85">1992</xref>; Woolfit and Bromham, <xref ref-type="bibr" rid="B117">2005</xref></td>
</tr>
<tr>
<td/>
<td align="center" valign="top">&#x0002B;</td>
<td align="left" valign="top">Diversity</td>
<td align="left" valign="top">Rate of molecular evolution</td>
<td align="left" valign="top">Duchene and Bromham, <xref ref-type="bibr" rid="B23">2013</xref></td>
</tr>
<tr>
<td align="left" valign="top">Trophic specialization</td>
<td align="center" valign="top">&#x02212;</td>
<td align="left" valign="top">Trophic specialization</td>
<td align="left" valign="top">Range size</td>
<td align="left" valign="top">Williams et al., <xref ref-type="bibr" rid="B116">2009</xref></td>
</tr>
<tr>
<td/>
<td align="center" valign="top">&#x02212;</td>
<td align="left" valign="top">Trophic specialization</td>
<td align="left" valign="top">Dispersal</td>
<td align="left" valign="top">Salisbury et al., <xref ref-type="bibr" rid="B98">2012</xref></td>
</tr>
<tr>
<td/>
<td align="center" valign="top">&#x0002B;</td>
<td align="left" valign="top">Trophic specialization</td>
<td align="left" valign="top">Intra-specific genetic structure</td>
<td align="left" valign="top">Hoffman et al., <xref ref-type="bibr" rid="B50">2005</xref>; Eastwood et al., <xref ref-type="bibr" rid="B26">2006</xref> Anton et al., <xref ref-type="bibr" rid="B3">2007</xref>; Habel et al., <xref ref-type="bibr" rid="B48">2009</xref></td>
</tr>
</tbody>
</table>
<table-wrap-foot>
<p><italic>Columns show the relationships documented in the literature that provide evidence for the proposed mechanism</italic>.</p>
</table-wrap-foot>
</table-wrap>
<sec>
<title>Conflict of interest statement</title>
<p>The author declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.</p></sec>
</sec>
</body>
<back>
<ack>
<p>Jens-Christian Svenning, Mary S. Wisz, Doyle McKay, Nadir Alvarez, Rudolf Rohr, Russell Naisbit, Nadine Sandau as well as the reviewers are thanked for their comments on a previous version of the manuscript.</p>
</ack>
<ref-list>
<title>References</title>
<ref id="B1">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Allen</surname> <given-names>A. P.</given-names></name> <name><surname>Gillooly</surname> <given-names>J. F.</given-names></name> <name><surname>Savage</surname> <given-names>V. M.</given-names></name> <name><surname>Brown</surname> <given-names>J. H.</given-names></name></person-group> (<year>2006</year>). <article-title>Kinetic effects of temperature on rates of genetic divergence and speciation</article-title>. <source>Proc. Natl. Acad. Sci. U.S.A</source>. <volume>103</volume>, <fpage>9130</fpage>&#x02013;<lpage>9135</lpage>. <pub-id pub-id-type="doi">10.1073/pnas.0603587103</pub-id><pub-id pub-id-type="pmid">16754845</pub-id></citation>
</ref>
<ref id="B2">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Allen</surname> <given-names>B.</given-names></name> <name><surname>Sample</surname> <given-names>C.</given-names></name> <name><surname>Dementieva</surname> <given-names>Y.</given-names></name> <name><surname>Medeiros</surname> <given-names>R. C.</given-names></name> <name><surname>Paoletti</surname> <given-names>C.</given-names></name> <name><surname>Nowak</surname> <given-names>M. A.</given-names></name></person-group> (<year>2015</year>). <article-title>The molecular clock of neutral evolution can be accelerated or slowed by asymmetric spatial structure</article-title>. <source>PLoS Comput. Biol</source>. <volume>11</volume>:<fpage>e1004108</fpage>. <pub-id pub-id-type="doi">10.1371/journal.pcbi.1004108</pub-id><pub-id pub-id-type="pmid">25719560</pub-id></citation>
</ref>
<ref id="B3">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Anton</surname> <given-names>C.</given-names></name> <name><surname>Zeisset</surname> <given-names>I.</given-names></name> <name><surname>Musche</surname> <given-names>M.</given-names></name> <name><surname>Durka</surname> <given-names>W.</given-names></name> <name><surname>Boomsma</surname> <given-names>J. J.</given-names></name> <name><surname>Settele</surname> <given-names>J.</given-names></name></person-group> (<year>2007</year>). <article-title>Population structure of a large blue butterfly and its specialist parasitoid in a fragmented landscape</article-title>. <source>Mol. Ecol</source>. <volume>16</volume>, <fpage>3828</fpage>&#x02013;<lpage>3838</lpage>. <pub-id pub-id-type="doi">10.1111/j.1365-294X.2007.03441.x</pub-id><pub-id pub-id-type="pmid">17850549</pub-id></citation>
</ref>
<ref id="B4">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Arenas</surname> <given-names>M.</given-names></name> <name><surname>Fran&#x000E7;ois</surname> <given-names>O.</given-names></name> <name><surname>Currat</surname> <given-names>M.</given-names></name> <name><surname>Ray</surname> <given-names>N.</given-names></name> <name><surname>Excoffier</surname> <given-names>L.</given-names></name></person-group> (<year>2013</year>). <article-title>Influence of admixture and Paleolithic range contractions on current European diversity gradients</article-title>. <source>Mol. Biol. Evol</source>. <volume>30</volume>, <fpage>57</fpage>&#x02013;<lpage>61</lpage>. <pub-id pub-id-type="doi">10.1093/molbev/mss203</pub-id><pub-id pub-id-type="pmid">22923464</pub-id></citation>
</ref>
<ref id="B5">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Arenas</surname> <given-names>M.</given-names></name> <name><surname>Ray</surname> <given-names>N.</given-names></name> <name><surname>Currat</surname> <given-names>M.</given-names></name> <name><surname>Excoffier</surname> <given-names>L.</given-names></name></person-group> (<year>2012</year>). <article-title>Consequences of range contractions and range shifts on molecular diversity</article-title>. <source>Mol. Biol. Evol</source>. <volume>29</volume>, <fpage>207</fpage>&#x02013;<lpage>218</lpage>. <pub-id pub-id-type="doi">10.1093/molbev/msr187</pub-id><pub-id pub-id-type="pmid">21778191</pub-id></citation>
</ref>
<ref id="B6">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Balloux</surname> <given-names>F.</given-names></name> <name><surname>Lehmann</surname> <given-names>L.</given-names></name></person-group> (<year>2012</year>). <article-title>Substitution rates at neutral genes depend on population size under fluctuating demography and overlapping generations</article-title>. <source>Evolution</source> <volume>66</volume>, <fpage>605</fpage>&#x02013;<lpage>611</lpage>. <pub-id pub-id-type="doi">10.1111/j.1558-5646.2011.01458.x</pub-id><pub-id pub-id-type="pmid">22276552</pub-id></citation>
</ref>
<ref id="B7">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Barluenga</surname> <given-names>M.</given-names></name> <name><surname>St&#x000F6;lting</surname> <given-names>K. N.</given-names></name> <name><surname>Salzburger</surname> <given-names>W.</given-names></name> <name><surname>Muschick</surname> <given-names>M.</given-names></name> <name><surname>Meyer</surname> <given-names>A.</given-names></name></person-group> (<year>2006</year>). <article-title>Sympatric speciation in Nicaraguan crater lake cichlid fish</article-title>. <source>Nature</source> <volume>439</volume>, <fpage>719</fpage>&#x02013;<lpage>723</lpage>. <pub-id pub-id-type="doi">10.1038/nature04325</pub-id><pub-id pub-id-type="pmid">16467837</pub-id></citation>
</ref>
<ref id="B8">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Bawa</surname> <given-names>K. S.</given-names></name></person-group> (<year>1974</year>). <article-title>Breeding systems of tree species of a lowland tropical community</article-title>. <source>Evolution</source> <volume>28</volume>, <fpage>85</fpage>&#x02013;<lpage>92</lpage>. <pub-id pub-id-type="doi">10.2307/2407241</pub-id></citation>
</ref>
<ref id="B9">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>B&#x000F6;hle</surname> <given-names>U. R.</given-names></name> <name><surname>Hilger</surname> <given-names>H. H.</given-names></name> <name><surname>Martin</surname> <given-names>W. F.</given-names></name></person-group> (<year>1996</year>). <article-title>Island colonization and evolution of the insular woody habit in Echium L. (Boraginaceae)</article-title>. <source>Proc. Natl. Acad. Sci. U.S.A</source>. <volume>93</volume>, <fpage>11740</fpage>&#x02013;<lpage>11745</lpage>. <pub-id pub-id-type="doi">10.1073/pnas.93.21.11740</pub-id><pub-id pub-id-type="pmid">8876207</pub-id></citation>
</ref>
<ref id="B10">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Born</surname> <given-names>C.</given-names></name> <name><surname>Hardy</surname> <given-names>O. J.</given-names></name> <name><surname>Chevallier</surname> <given-names>M. H.</given-names></name> <name><surname>Ossari</surname> <given-names>S.</given-names></name> <name><surname>Atteke</surname> <given-names>C.</given-names></name> <name><surname>Wickings</surname> <given-names>E.</given-names></name> <etal/></person-group>. (<year>2008</year>). <article-title>Small&#x02212;scale spatial genetic structure in the Central African rainforest tree species <italic>Aucoumea klaineana</italic>: a stepwise approach to infer the impact of limited gene dispersal, population history and habitat fragmentation</article-title>. <source>Mol. Ecol</source>. <volume>17</volume>, <fpage>2041</fpage>&#x02013;<lpage>2050</lpage>. <pub-id pub-id-type="doi">10.1111/j.1365-294X.2007.03685.x</pub-id><pub-id pub-id-type="pmid">18331246</pub-id></citation>
</ref>
<ref id="B11">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Bromham</surname> <given-names>L.</given-names></name></person-group> (<year>2002</year>). <article-title>Molecular clocks in reptiles: life history influences rate of molecular evolution</article-title>. <source>Mol. Biol. Evol</source>. <volume>19</volume>, <fpage>302</fpage>&#x02013;<lpage>309</lpage>. <pub-id pub-id-type="doi">10.1093/oxfordjournals.molbev.a004083</pub-id><pub-id pub-id-type="pmid">11861889</pub-id></citation>
</ref>
<ref id="B12">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Bromham</surname> <given-names>L.</given-names></name> <name><surname>Hua</surname> <given-names>X.</given-names></name> <name><surname>Lanfear</surname> <given-names>R.</given-names></name> <name><surname>Cowman</surname> <given-names>P. F.</given-names></name></person-group> (<year>2015</year>). <article-title>Exploring the relationships between mutation rates, life history, genome size, environment, and species richness in flowering plants</article-title>. <source>Am. Nat</source>. <volume>185</volume>, <fpage>507</fpage>&#x02013;<lpage>524</lpage>. <pub-id pub-id-type="doi">10.1086/680052</pub-id><pub-id pub-id-type="pmid">25811085</pub-id></citation>
</ref>
<ref id="B13">
<citation citation-type="book"><person-group person-group-type="author"><name><surname>Brown</surname> <given-names>J. H.</given-names></name> <name><surname>Gibson</surname> <given-names>A. C.</given-names></name></person-group> (<year>1983</year>). <source>Biogeography</source>. <publisher-loc>St.Louis, MO</publisher-loc>: <publisher-name>Mosby</publisher-name>.</citation>
</ref>
<ref id="B14">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Burns</surname> <given-names>J. M.</given-names></name> <name><surname>Janzen</surname> <given-names>D. H.</given-names></name> <name><surname>Hajibabaei</surname> <given-names>M.</given-names></name> <name><surname>Hallwachs</surname> <given-names>W.</given-names></name> <name><surname>Hebert</surname> <given-names>P. D. N.</given-names></name></person-group> (<year>2008</year>). <article-title>DNA barcodes and cryptic species of skipper butterflies in the genus Perichares in Area de Conservacion Guanacaste, Costa Rica</article-title>. <source>Proc. Natl. Acad. Sci. U.S.A</source>. <volume>105</volume>, <fpage>6350</fpage>&#x02013;<lpage>6355</lpage>. <pub-id pub-id-type="doi">10.1073/pnas.0712181105</pub-id><pub-id pub-id-type="pmid">18436645</pub-id></citation>
</ref>
<ref id="B15">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Bush</surname> <given-names>G. L.</given-names></name> <name><surname>Case</surname> <given-names>S. M.</given-names></name> <name><surname>Wilson</surname> <given-names>A. C.</given-names></name> <name><surname>Patton</surname> <given-names>J. L.</given-names></name></person-group> (<year>1977</year>). <article-title>Rapid speciation and chromosomal evolution in mammals</article-title>. <source>Proc. Natl. Acad. Sci. U.S.A</source>. <volume>74</volume>, <fpage>3942</fpage>&#x02013;<lpage>3946</lpage>. <pub-id pub-id-type="doi">10.1073/pnas.74.9.3942</pub-id><pub-id pub-id-type="pmid">269445</pub-id></citation>
</ref>
<ref id="B16">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Cadotte</surname> <given-names>M. W.</given-names></name> <name><surname>Mai</surname> <given-names>D. V.</given-names></name> <name><surname>Jantz</surname> <given-names>S.</given-names></name> <name><surname>Collins</surname> <given-names>M. D.</given-names></name> <name><surname>Keele</surname> <given-names>M.</given-names></name> <name><surname>Drake</surname> <given-names>J. A.</given-names></name></person-group> (<year>2006</year>). <article-title>On testing the competition-colonization trade-off in a multispecies assemblage</article-title>. <source>Am. Nat</source>. <volume>168</volume>, <fpage>704</fpage>&#x02013;<lpage>709</lpage>. <pub-id pub-id-type="doi">10.1086/508296</pub-id><pub-id pub-id-type="pmid">17080367</pub-id></citation>
</ref>
<ref id="B17">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Calcagno</surname> <given-names>V.</given-names></name> <name><surname>Mouquet</surname> <given-names>N.</given-names></name> <name><surname>Jarne</surname> <given-names>P.</given-names></name> <name><surname>David</surname> <given-names>P.</given-names></name></person-group> (<year>2006</year>). <article-title>Coexistence in a metacommunity: the competition&#x02013;colonization trade&#x02212;off is not dead</article-title>. <source>Ecol. Lett</source>. <volume>9</volume>, <fpage>897</fpage>&#x02013;<lpage>907</lpage>. <pub-id pub-id-type="doi">10.1111/j.1461-0248.2006.00930.x</pub-id><pub-id pub-id-type="pmid">16913929</pub-id></citation>
</ref>
<ref id="B18">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Cardillo</surname> <given-names>M.</given-names></name></person-group> (<year>1999</year>). <article-title>Latitude and rates of diversification in birds and butterflies</article-title>. <source>Proc. R. Soc. B Biol. Sci</source>. <volume>266</volume>, <fpage>1221</fpage>. <pub-id pub-id-type="doi">10.1098/rspb.1999.0766</pub-id></citation>
</ref>
<ref id="B19">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Charlesworth</surname> <given-names>B.</given-names></name></person-group> (<year>2009</year>). <article-title>Fundamental concepts in genetics: effective population size and patterns of molecular evolution and variation</article-title>. <source>Nat. Rev. Genet</source>. <volume>10</volume>, <fpage>195</fpage>&#x02013;<lpage>205</lpage>. <pub-id pub-id-type="doi">10.1038/nrg2526</pub-id><pub-id pub-id-type="pmid">19204717</pub-id></citation>
</ref>
<ref id="B20">
<citation citation-type="book"><person-group person-group-type="author"><name><surname>Darwin</surname> <given-names>C.</given-names></name></person-group> (<year>1859</year>). <source>On the Origins of Species by means of Natural Selection</source>. <publisher-loc>London</publisher-loc>: <publisher-name>Murray</publisher-name>.</citation>
</ref>
<ref id="B21">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Dobzhansky</surname> <given-names>T.</given-names></name></person-group> (<year>1950</year>). <article-title>Evolution in the tropics</article-title>. <source>Am. Sci</source>. <volume>38</volume>, <fpage>209</fpage>&#x02013;<lpage>221</lpage>.</citation>
</ref>
<ref id="B22">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Dowle</surname> <given-names>E. J.</given-names></name> <name><surname>Morgan-Richards</surname> <given-names>M.</given-names></name> <name><surname>Trewick</surname> <given-names>S. A.</given-names></name></person-group> (<year>2013</year>). <article-title>Molecular evolution and the latitudinal biodiversity gradient</article-title>. <source>Heredity</source> <volume>110</volume>, <fpage>501</fpage>&#x02013;<lpage>510</lpage>. <pub-id pub-id-type="doi">10.1038/hdy.2013.4</pub-id><pub-id pub-id-type="pmid">23486082</pub-id></citation>
</ref>
<ref id="B23">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Duchene</surname> <given-names>D.</given-names></name> <name><surname>Bromham</surname> <given-names>L.</given-names></name></person-group> (<year>2013</year>). <article-title>Rates of molecular evolution and diversification in plants: chloroplast substitution rates correlated with species-richness in the Proteaceae</article-title>. <source>BMC Evol. Biol</source>. <volume>13</volume>:<fpage>65</fpage>. <pub-id pub-id-type="doi">10.1186/1471-2148-13-65</pub-id><pub-id pub-id-type="pmid">23497266</pub-id></citation>
</ref>
<ref id="B24">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Duminil</surname> <given-names>J.</given-names></name> <name><surname>Fineschi</surname> <given-names>S.</given-names></name> <name><surname>Hampe</surname> <given-names>A.</given-names></name> <name><surname>Jordano</surname> <given-names>P.</given-names></name> <name><surname>Salvini</surname> <given-names>D.</given-names></name> <name><surname>Vendramin</surname> <given-names>G. G.</given-names></name> <etal/></person-group>. (<year>2007</year>). <article-title>Can population genetic structure be predicted from life&#x02212;history traits?</article-title> <source>Am. Nat</source>. <volume>169</volume>, <fpage>662</fpage>&#x02013;<lpage>672</lpage>. <pub-id pub-id-type="doi">10.1086/513490</pub-id><pub-id pub-id-type="pmid">17427136</pub-id></citation>
</ref>
<ref id="B25">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Dynesius</surname> <given-names>M.</given-names></name> <name><surname>Jansson</surname> <given-names>R.</given-names></name></person-group> (<year>2000</year>). <article-title>Evolutionary consequences of changes in species&#x00027; geographical distributions driven by Milankovitch climate oscillations</article-title>. <source>Proc. Natl. Acad. Sci. U.S.A</source>. <volume>97</volume>, <fpage>9115</fpage>&#x02013;<lpage>9120</lpage>. <pub-id pub-id-type="doi">10.1073/pnas.97.16.9115</pub-id><pub-id pub-id-type="pmid">10922067</pub-id></citation>
</ref>
<ref id="B26">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Eastwood</surname> <given-names>R.</given-names></name> <name><surname>Pierce</surname> <given-names>N. E.</given-names></name> <name><surname>Kitching</surname> <given-names>R. L.</given-names></name> <name><surname>Hughes</surname> <given-names>J. M.</given-names></name></person-group> (<year>2006</year>). <article-title>Do ants enhance diversification in lycaenid butterflies? Phylogeographic evidence from a model myrmecophile, Jalmenus evagoras</article-title>. <source>Evolution</source> <volume>60</volume>, <fpage>315</fpage>&#x02013;<lpage>327</lpage>. <pub-id pub-id-type="doi">10.1111/j.0014-3820.2006.tb01109.x</pub-id><pub-id pub-id-type="pmid">16610323</pub-id></citation>
</ref>
<ref id="B27">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Ehrl&#x000E9;n</surname> <given-names>J.</given-names></name> <name><surname>Groenendael</surname> <given-names>J. M.</given-names></name></person-group> (<year>1998</year>). <article-title>The trade-off between dispersability and longevity-an important aspect of plant species diversity</article-title>. <source>Appl. Veg. Sci</source>. <volume>1</volume>, <fpage>29</fpage>&#x02013;<lpage>36</lpage>. <pub-id pub-id-type="doi">10.2307/1479083</pub-id></citation>
</ref>
<ref id="B28">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Eldredge</surname> <given-names>N.</given-names></name> <name><surname>Thompson</surname> <given-names>J. N.</given-names></name> <name><surname>Brakefield</surname> <given-names>P. M.</given-names></name> <name><surname>Gavrilets</surname> <given-names>S.</given-names></name> <name><surname>Jablonski</surname> <given-names>D.</given-names></name> <name><surname>Jackson</surname> <given-names>J. B. C.</given-names></name> <etal/></person-group>. (<year>2005</year>). <article-title>The dynamics of evolutionary stasis</article-title>. <source>Paleobiology</source> <volume>31</volume>, <fpage>133</fpage>&#x02013;<lpage>145</lpage>. <pub-id pub-id-type="doi">10.1666/0094-8373(2005)031[0133:TDOES]2.0.CO;2</pub-id></citation>
</ref>
<ref id="B29">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Emerson</surname> <given-names>B. C.</given-names></name> <name><surname>Kolm</surname> <given-names>N.</given-names></name></person-group> (<year>2005</year>). <article-title>Species diversity can drive speciation</article-title>. <source>Nature</source> <volume>434</volume>, <fpage>1015</fpage>&#x02013;<lpage>1017</lpage>. <pub-id pub-id-type="doi">10.1038/nature03450</pub-id><pub-id pub-id-type="pmid">15846345</pub-id></citation>
</ref>
<ref id="B30">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Eo</surname> <given-names>S. H.</given-names></name> <name><surname>DeWoody</surname> <given-names>J. A.</given-names></name></person-group> (<year>2010</year>). <article-title>Evolutionary rates of mitochondrial genomes correspond to diversification rates and to contemporary species richness in birds and reptiles</article-title>. <source>Proc. Biol. Sci</source>. <volume>277</volume>, <fpage>3587</fpage>&#x02013;<lpage>3592</lpage>. <pub-id pub-id-type="doi">10.1098/rspb.2010.0965</pub-id><pub-id pub-id-type="pmid">20610427</pub-id></citation>
</ref>
<ref id="B31">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Eo</surname> <given-names>S. H.</given-names></name> <name><surname>Wares</surname> <given-names>J. P.</given-names></name> <name><surname>Carroll</surname> <given-names>J. P.</given-names></name></person-group> (<year>2008</year>). <article-title>Population divergence in plant species reflects latitudinal biodiversity gradients</article-title>. <source>Biol. Lett</source>. <volume>4</volume>, <fpage>382</fpage>&#x02013;<lpage>384</lpage>. <pub-id pub-id-type="doi">10.1098/rsbl.2008.0109</pub-id><pub-id pub-id-type="pmid">18492649</pub-id></citation>
</ref>
<ref id="B32">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Excoffier</surname> <given-names>L.</given-names></name> <name><surname>Ray</surname> <given-names>N.</given-names></name></person-group> (<year>2008</year>). <article-title>Surfing during population expansions promotes genetic revolutions and structuration</article-title>. <source>Trends Ecol. Evol</source>. <volume>23</volume>, <fpage>347</fpage>&#x02013;<lpage>351</lpage>. <pub-id pub-id-type="doi">10.1016/j.tree.2008.04.004</pub-id><pub-id pub-id-type="pmid">18502536</pub-id></citation>
</ref>
<ref id="B33">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Fedorov</surname> <given-names>A. A.</given-names></name></person-group> (<year>1966</year>). <article-title>The structure of the tropical rain forest and speciation in the humid tropics</article-title>. <source>J. Ecol</source>. <volume>1</volume>, <fpage>1</fpage>&#x02013;<lpage>11</lpage>. <pub-id pub-id-type="doi">10.2307/2257656</pub-id></citation>
</ref>
<ref id="B34">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Forister</surname> <given-names>M. L.</given-names></name> <name><surname>Dyer</surname> <given-names>L. A.</given-names></name> <name><surname>Singer</surname> <given-names>M. S.</given-names></name> <name><surname>Stireman</surname> <given-names>J. O.</given-names></name> <name><surname>Lill</surname> <given-names>J. T.</given-names></name></person-group> (<year>2012</year>). <article-title>Revisiting the evolution of ecological specialization, with emphasis on insect-plant interactions</article-title>. <source>Ecology</source> <volume>93</volume>, <fpage>981</fpage>&#x02013;<lpage>991</lpage>. <pub-id pub-id-type="doi">10.1890/11-0650.1</pub-id><pub-id pub-id-type="pmid">22764485</pub-id></citation>
</ref>
<ref id="B35">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Futuyma</surname> <given-names>D. J.</given-names></name> <name><surname>Moreno</surname> <given-names>G.</given-names></name></person-group> (<year>1988</year>). <article-title>The evolution of ecological specialization</article-title>. <source>Annu. Rev. Ecol. Syst</source>. <volume>19</volume>, <fpage>207</fpage>&#x02013;<lpage>233</lpage>. <pub-id pub-id-type="doi">10.1146/annurev.es.19.110188.001231</pub-id></citation>
</ref>
<ref id="B36">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Gaston</surname> <given-names>K. J.</given-names></name></person-group> (<year>1998</year>). <article-title>Species-range size distributions: products of speciation, extinction and transformation</article-title>. <source>Philos. Trans. R. Soc. B Biol. Sci</source>. <volume>353</volume>, <fpage>219</fpage>&#x02013;<lpage>230</lpage>. <pub-id pub-id-type="doi">10.1098/rstb.1998.0204</pub-id></citation>
</ref>
<ref id="B37">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Gaston</surname> <given-names>K. J.</given-names></name></person-group> (<year>2000</year>). <article-title>Global patterns in biodiversity</article-title>. <source>Nature</source> <volume>405</volume>, <fpage>220</fpage>&#x02013;<lpage>227</lpage>. <pub-id pub-id-type="doi">10.1038/35012228</pub-id><pub-id pub-id-type="pmid">10821282</pub-id></citation>
</ref>
<ref id="B38">
<citation citation-type="book"><person-group person-group-type="author"><name><surname>Gavrilets</surname> <given-names>S.</given-names></name></person-group> (<year>2004</year>). <source>Fitness Landscapes and the Origin of Species</source>. <publisher-loc>Princeton, NJ</publisher-loc>: <publisher-name>Princeton university press</publisher-name>.</citation>
</ref>
<ref id="B39">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Gavrilets</surname> <given-names>S.</given-names></name></person-group> (<year>2014</year>). <article-title>Models of speciation: where are we now?</article-title> <source>J. Hered</source>. <volume>105</volume>, <fpage>743</fpage>&#x02013;<lpage>755</lpage>. <pub-id pub-id-type="doi">10.1093/jhered/esu045</pub-id><pub-id pub-id-type="pmid">25149251</pub-id></citation>
</ref>
<ref id="B40">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Gavrilets</surname> <given-names>S.</given-names></name> <name><surname>Gibson</surname> <given-names>N.</given-names></name></person-group> (<year>2002</year>). <article-title>Fixation probabilities in a spatially heterogeneous environment</article-title>. <source>Popul. Ecol</source>. <volume>44</volume>, <fpage>51</fpage>&#x02013;<lpage>58</lpage>. <pub-id pub-id-type="doi">10.1007/s101440200007</pub-id></citation>
</ref>
<ref id="B41">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Gavrilets</surname> <given-names>S.</given-names></name> <name><surname>Li</surname> <given-names>H.</given-names></name> <name><surname>Vose</surname> <given-names>M. D.</given-names></name></person-group> (<year>2000</year>). <article-title>Patterns of parapatric speciation</article-title>. <source>Evolution</source> <volume>54</volume>, <fpage>1126</fpage>&#x02013;<lpage>1134</lpage>. <pub-id pub-id-type="doi">10.1111/j.0014-3820.2000.tb00548.x</pub-id><pub-id pub-id-type="pmid">11005282</pub-id></citation>
</ref>
<ref id="B42">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Gillman</surname> <given-names>L. N.</given-names></name> <name><surname>Keeling</surname> <given-names>D. J.</given-names></name> <name><surname>Ross</surname> <given-names>H. A.</given-names></name> <name><surname>Wright</surname> <given-names>S. D.</given-names></name></person-group> (<year>2009</year>). <article-title>Latitude, elevation and the tempo of molecular evolution in mammals</article-title>. <source>Proc. Biol. Sci</source>. <volume>276</volume>, <fpage>3353</fpage>&#x02013;<lpage>3359</lpage>. <pub-id pub-id-type="doi">10.1098/rspb.2009.0674</pub-id><pub-id pub-id-type="pmid">19556254</pub-id></citation>
</ref>
<ref id="B43">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Gillman</surname> <given-names>L. N.</given-names></name> <name><surname>McCowan</surname> <given-names>L. S. C.</given-names></name> <name><surname>Wright</surname> <given-names>S. D.</given-names></name></person-group> (<year>2012</year>). <article-title>The tempo of genetic evolution in birds: body mass and climate effects</article-title>. <source>J. Biogeogr</source>. <volume>39</volume>, <fpage>1567</fpage>&#x02013;<lpage>1572</lpage>. <pub-id pub-id-type="doi">10.1111/j.1365-2699.2012.02730.x</pub-id></citation>
</ref>
<ref id="B44">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Gillooly</surname> <given-names>J. F.</given-names></name> <name><surname>Allen</surname> <given-names>A. P.</given-names></name></person-group> (<year>2007</year>). <article-title>Linking global patterns in biodiversity to evolutionary dynamics using metabolic theory</article-title>. <source>Ecology</source> <volume>88</volume>, <fpage>1890</fpage>&#x02013;<lpage>1894</lpage>. <pub-id pub-id-type="doi">10.1890/06-1935.1</pub-id><pub-id pub-id-type="pmid">17824416</pub-id></citation>
</ref>
<ref id="B45">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Gould</surname> <given-names>S. J.</given-names></name> <name><surname>Eldredge</surname> <given-names>N.</given-names></name></person-group> (<year>1977</year>). <article-title>Punctuated equilibria: the tempo and mode of evolution reconsidered</article-title>. <source>Paleobiology</source> <volume>3</volume>, <fpage>115</fpage>&#x02013;<lpage>151</lpage>.</citation>
</ref>
<ref id="B46">
<citation citation-type="book"><person-group person-group-type="author"><name><surname>Grant</surname> <given-names>P. R.</given-names></name> <name><surname>Grant</surname> <given-names>B. R.</given-names></name></person-group> (<year>2011</year>). <source>How and Why Species Multiply: the Radiation of Darwin&#x00027;s Finches</source>. <publisher-loc>New Jersey</publisher-loc>: <publisher-name>Princeton University Press</publisher-name>.</citation>
</ref>
<ref id="B47">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Grime</surname> <given-names>J. P.</given-names></name></person-group> (<year>1977</year>). <article-title>Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory</article-title>. <source>Am. Nat</source>. <volume>111</volume>, <fpage>1169</fpage>. <pub-id pub-id-type="doi">10.1086/283244</pub-id></citation>
</ref>
<ref id="B48">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Habel</surname> <given-names>J. C.</given-names></name> <name><surname>Meyer</surname> <given-names>M.</given-names></name> <name><surname>Schmitt</surname> <given-names>T.</given-names></name></person-group> (<year>2009</year>). <article-title>The genetic consequence of differing ecological demands of a generalist and a specialist butterfly species</article-title>. <source>Biodivers. Conserv</source>. <volume>18</volume>, <fpage>1895</fpage>&#x02013;<lpage>1908</lpage>. <pub-id pub-id-type="doi">10.1007/s10531-008-9563-5</pub-id></citation>
</ref>
<ref id="B49">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Hardy</surname> <given-names>O. J.</given-names></name> <name><surname>Maggia</surname> <given-names>L.</given-names></name> <name><surname>Bandou</surname> <given-names>E.</given-names></name> <name><surname>Breyne</surname> <given-names>P.</given-names></name> <name><surname>Caron</surname> <given-names>H.</given-names></name> <name><surname>Chevallier</surname> <given-names>M. H.</given-names></name> <etal/></person-group>. (<year>2006</year>). <article-title>Fine-scale genetic structure and gene dispersal inferences in 10 Neotropical tree species</article-title>. <source>Mol. Ecol</source>. <volume>15</volume>, <fpage>559</fpage>&#x02013;<lpage>571</lpage>. <pub-id pub-id-type="doi">10.1111/j.1365-294X.2005.02785.x</pub-id><pub-id pub-id-type="pmid">16448421</pub-id></citation>
</ref>
<ref id="B50">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Hoffman</surname> <given-names>E. A.</given-names></name> <name><surname>Kolm</surname> <given-names>N.</given-names></name> <name><surname>Berglund</surname> <given-names>A.</given-names></name> <name><surname>Arguello</surname> <given-names>J. R.</given-names></name> <name><surname>Jones</surname> <given-names>A. G.</given-names></name></person-group> (<year>2005</year>). <article-title>Genetic structure in the coral-reef-associated Banggai cardinalfish, <italic>Pterapogon kauderni</italic></article-title>. <source>Mol. Ecol</source>. <volume>14</volume>, <fpage>1367</fpage>&#x02013;<lpage>1375</lpage>. <pub-id pub-id-type="doi">10.1111/j.1365-294X.2005.02538.x</pub-id><pub-id pub-id-type="pmid">15813777</pub-id></citation>
</ref>
<ref id="B51">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Hopkins</surname> <given-names>M. J.</given-names></name></person-group> (<year>2011</year>). <article-title>How species longevity, intraspecific morphological variation, and geographic range size are related: a comparison using Late Cambrian trilobites</article-title>. <source>Evolution</source> <volume>65</volume>, <fpage>3253</fpage>&#x02013;<lpage>3273</lpage>. <pub-id pub-id-type="doi">10.1111/j.1558-5646.2011.01379.x</pub-id><pub-id pub-id-type="pmid">22023590</pub-id></citation>
</ref>
<ref id="B52">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Hopkins</surname> <given-names>R.</given-names></name></person-group> (<year>2013</year>). <article-title>Reinforcement in plants</article-title>. <source>New Phytol</source>. <volume>197</volume>, <fpage>1095</fpage>&#x02013;<lpage>1103</lpage>. <pub-id pub-id-type="doi">10.1111/nph.12119</pub-id><pub-id pub-id-type="pmid">23495388</pub-id></citation>
</ref>
<ref id="B53">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Horn</surname> <given-names>H. S.</given-names></name></person-group> (<year>1974</year>). <article-title>The ecology of secondary succession</article-title>. <source>Annu. Rev. Ecol. Syst</source>. <volume>5</volume>, <fpage>25</fpage>&#x02013;<lpage>37</lpage>. <pub-id pub-id-type="doi">10.1146/annurev.es.05.110174.000325</pub-id></citation>
</ref>
<ref id="B54">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Hubbell</surname> <given-names>S. P.</given-names></name></person-group> (<year>1979</year>). <article-title>Tree dispersion, abundance, and diversity in a tropical dry forest</article-title>. <source>Science</source> <volume>203</volume>, <fpage>1299</fpage>&#x02013;<lpage>1309</lpage>. <pub-id pub-id-type="doi">10.1126/science.203.4387.1299</pub-id><pub-id pub-id-type="pmid">17780463</pub-id></citation>
</ref>
<ref id="B55">
<citation citation-type="book"><person-group person-group-type="author"><name><surname>Hubbell</surname> <given-names>S. P.</given-names></name></person-group> (<year>2001</year>). <source>The Unified Neutral Theory of Biodiversity and Biogeography</source>. <publisher-loc>New Jersey</publisher-loc>: <publisher-name>Princeton University Press</publisher-name>.</citation>
</ref>
<ref id="B56">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Jablonski</surname> <given-names>D.</given-names></name></person-group> (<year>2007</year>). <article-title>Scale and hierarchy in macroevolution</article-title>. <source>Palaeontology</source> <volume>50</volume>, <fpage>87</fpage>&#x02013;<lpage>109</lpage>. <pub-id pub-id-type="doi">10.1111/j.1475-4983.2006.00615.x</pub-id></citation>
</ref>
<ref id="B57">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Jablonski</surname> <given-names>D.</given-names></name></person-group> (<year>2008</year>). <article-title>Extinction and the spatial dynamics of biodiversity</article-title>. <source>Proc. Natl. Acad. Sci. U.S.A</source>. <volume>105</volume>, <fpage>11528</fpage>&#x02013;<lpage>11535</lpage>. <pub-id pub-id-type="doi">10.1073/pnas.0801919105</pub-id><pub-id pub-id-type="pmid">18695229</pub-id></citation>
</ref>
<ref id="B58">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Jablonski</surname> <given-names>D.</given-names></name> <name><surname>Roy</surname> <given-names>K.</given-names></name></person-group> (<year>2003</year>). <article-title>Geographical range and speciation in fossil and living molluscs</article-title>. <source>Proc. Biol. Sci</source>. <volume>270</volume>, <fpage>401</fpage>&#x02013;<lpage>406</lpage>. <pub-id pub-id-type="doi">10.1098/rspb.2002.2243</pub-id><pub-id pub-id-type="pmid">12639320</pub-id></citation>
</ref>
<ref id="B59">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Janzen</surname> <given-names>D. H.</given-names></name></person-group> (<year>1968</year>). <article-title>Host plants as islands in evolutionary and contemporary time</article-title>. <source>Am. Nat</source>. <volume>102</volume>, <fpage>592</fpage>&#x02013;<lpage>595</lpage>. <pub-id pub-id-type="doi">10.1086/282574</pub-id><pub-id pub-id-type="pmid">25061680</pub-id></citation>
</ref>
<ref id="B60">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Jocque</surname> <given-names>M.</given-names></name> <name><surname>Field</surname> <given-names>R.</given-names></name> <name><surname>Brendonck</surname> <given-names>L.</given-names></name> <name><surname>De Meester</surname> <given-names>L.</given-names></name></person-group> (<year>2010</year>). <article-title>Climatic control of dispersal-ecological specialization trade-offs: a metacommunity process at the heart of the latitudinal diversity gradient?</article-title> <source>Glob. Ecol. Biogeogr</source>. <volume>19</volume>, <fpage>244</fpage>&#x02013;<lpage>252</lpage>. <pub-id pub-id-type="doi">10.1111/j.1466-8238.2009.00510.x</pub-id></citation>
</ref>
<ref id="B61">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Johnson</surname> <given-names>K. P.</given-names></name> <name><surname>Seger</surname> <given-names>J.</given-names></name></person-group> (<year>2001</year>). <article-title>Elevated rates of nonsynonymous substitution in island birds</article-title>. <source>Mol. Biol. Evol</source>. <volume>18</volume>, <fpage>874</fpage>&#x02013;<lpage>881</lpage>. <pub-id pub-id-type="doi">10.1093/oxfordjournals.molbev.a003869</pub-id><pub-id pub-id-type="pmid">11319271</pub-id></citation>
</ref>
<ref id="B62">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Kimura</surname> <given-names>M.</given-names></name></person-group> (<year>1957</year>). <article-title>Some problems of stochastic processes in genetics</article-title>. <source>Ann. Math. Stat</source>. <volume>4</volume>, <fpage>882</fpage>&#x02013;<lpage>901</lpage>. <pub-id pub-id-type="doi">10.1214/aoms/1177706791</pub-id></citation>
</ref>
<ref id="B63">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Kisel</surname> <given-names>Y.</given-names></name> <name><surname>Barraclough</surname> <given-names>T. G.</given-names></name></person-group> (<year>2010</year>). <article-title>Speciation has a spatial scale that depends on levels of gene flow</article-title>. <source>Am. Nat</source>. <volume>175</volume>, <fpage>316</fpage>&#x02013;<lpage>334</lpage>. <pub-id pub-id-type="doi">10.1086/650369</pub-id><pub-id pub-id-type="pmid">20100106</pub-id></citation>
</ref>
<ref id="B64">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Kreft</surname> <given-names>H.</given-names></name> <name><surname>Jetz</surname> <given-names>W.</given-names></name></person-group> (<year>2007</year>). <article-title>Global patterns and determinants of vascular plant diversity</article-title>. <source>Proc. Natl. Acad. Sci. U.S.A</source>. <volume>104</volume>, <fpage>5925</fpage>&#x02013;<lpage>5930</lpage>. <pub-id pub-id-type="doi">10.1073/pnas.0608361104</pub-id><pub-id pub-id-type="pmid">17379667</pub-id></citation>
</ref>
<ref id="B65">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Kryazhimskiy</surname> <given-names>S.</given-names></name> <name><surname>Plotkin</surname> <given-names>J. B.</given-names></name></person-group> (<year>2008</year>). <article-title>The population genetics of dN/dS</article-title>. <source>PLoS Genet</source>. <volume>4</volume>:<fpage>e1000304</fpage>. <pub-id pub-id-type="doi">10.1371/journal.pgen.1000304</pub-id><pub-id pub-id-type="pmid">19081788</pub-id></citation>
</ref>
<ref id="B66">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Lanfear</surname> <given-names>R.</given-names></name> <name><surname>Ho</surname> <given-names>S. Y.</given-names></name> <name><surname>Love</surname> <given-names>D.</given-names></name> <name><surname>Bromham</surname> <given-names>L.</given-names></name></person-group> (<year>2010</year>). <article-title>Mutation rate is linked to diversification in birds</article-title>. <source>Proc. Natl. Acad. Sci. U.S.A</source>. <volume>107</volume>, <fpage>20423</fpage>&#x02013;<lpage>20428</lpage>. <pub-id pub-id-type="doi">10.1073/pnas.1007888107</pub-id><pub-id pub-id-type="pmid">21059910</pub-id></citation>
</ref>
<ref id="B67">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Lanfear</surname> <given-names>R.</given-names></name> <name><surname>Ho</surname> <given-names>S. Y. W.</given-names></name> <name><surname>Jonathan Davies</surname> <given-names>T.</given-names></name> <name><surname>Moles</surname> <given-names>A. T.</given-names></name> <name><surname>Aarssen</surname> <given-names>L.</given-names></name> <name><surname>Swenson</surname> <given-names>N. G.</given-names></name> <etal/></person-group>. (<year>2013</year>). <article-title>Taller plants have lower rates of molecular evolution</article-title>. <source>Nat. Commun</source>. <volume>4</volume>:<fpage>1879</fpage>. <pub-id pub-id-type="doi">10.1038/ncomms2836</pub-id><pub-id pub-id-type="pmid">23695673</pub-id></citation>
</ref>
<ref id="B68">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Lanfear</surname> <given-names>R.</given-names></name> <name><surname>Kokko</surname> <given-names>H.</given-names></name> <name><surname>Eyre-Walker</surname> <given-names>A.</given-names></name></person-group> (<year>2014</year>). <article-title>Population size and the rate of evolution</article-title>. <source>Trends Ecol. Evol</source>. <volume>29</volume>, <fpage>33</fpage>&#x02013;<lpage>41</lpage>. <pub-id pub-id-type="doi">10.1016/j.tree.2013.09.009</pub-id><pub-id pub-id-type="pmid">24148292</pub-id></citation>
</ref>
<ref id="B69">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Lasso</surname> <given-names>E.</given-names></name> <name><surname>Dalling</surname> <given-names>J. W.</given-names></name> <name><surname>Bermingham</surname> <given-names>E.</given-names></name></person-group> (<year>2011</year>). <article-title>Strong spatial genetic structure in five tropical Piper species: should the Baker&#x02013;Fedorov hypothesis be revived for tropical shrubs?</article-title> <source>Ecol. Evol</source>. <volume>1</volume>, <fpage>502</fpage>&#x02013;<lpage>516</lpage>. <pub-id pub-id-type="doi">10.1002/ece3.40</pub-id><pub-id pub-id-type="pmid">22393518</pub-id></citation>
</ref>
<ref id="B70">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Lester</surname> <given-names>S. E.</given-names></name> <name><surname>Ruttenberg</surname> <given-names>B. I.</given-names></name> <name><surname>Gaines</surname> <given-names>S. D.</given-names></name> <name><surname>Kinlan</surname> <given-names>B. P.</given-names></name></person-group> (<year>2007</year>). <article-title>The relationship between dispersal ability and geographic range size</article-title>. <source>Ecol. Lett</source>. <volume>10</volume>, <fpage>745</fpage>&#x02013;<lpage>758</lpage>. <pub-id pub-id-type="doi">10.1111/j.1461-0248.2007.01070.x</pub-id><pub-id pub-id-type="pmid">17594430</pub-id></citation>
</ref>
<ref id="B71">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Levin</surname> <given-names>D. A.</given-names></name></person-group> (<year>1993</year>). <article-title>Local speciation in plants: the rule not exception</article-title>. <source>Syst. Biol</source>. <volume>18</volume>, <fpage>197</fpage>&#x02013;<lpage>208</lpage>.</citation>
</ref>
<ref id="B72">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Levins</surname> <given-names>R.</given-names></name> <name><surname>Culver</surname> <given-names>D.</given-names></name></person-group> (<year>1971</year>). <article-title>Regional coexistence of species and competition between rare species</article-title>. <source>Proc. Natl. Acad. Sci. U.S.A</source>. <volume>68</volume>, <fpage>1246</fpage>&#x02013;<lpage>1248</lpage>. <pub-id pub-id-type="doi">10.1073/pnas.68.6.1246</pub-id><pub-id pub-id-type="pmid">16591932</pub-id></citation>
</ref>
<ref id="B73">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Litsios</surname> <given-names>G.</given-names></name> <name><surname>Sims</surname> <given-names>C. A.</given-names></name> <name><surname>W&#x000FC;est</surname> <given-names>R. O.</given-names></name> <name><surname>Pearman</surname> <given-names>P. B.</given-names></name> <name><surname>Zimmermann</surname> <given-names>N. E.</given-names></name> <name><surname>Salamin</surname> <given-names>N.</given-names></name></person-group> (<year>2012</year>). <article-title>Mutualism with sea anemones triggered the adaptive radiation of clownfishes</article-title>. <source>BMC Evol. Biol</source>. <volume>12</volume>:<fpage>212</fpage>. <pub-id pub-id-type="doi">10.1186/1471-2148-12-212</pub-id><pub-id pub-id-type="pmid">23122007</pub-id></citation>
</ref>
<ref id="B74">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Losos</surname> <given-names>J. B.</given-names></name></person-group> (<year>1998</year>). <article-title>Contingency and determinism in replicated adaptive radiations of island lizards</article-title>. <source>Science</source> <volume>279</volume>, <fpage>2115</fpage>&#x02013;<lpage>2118</lpage>. <pub-id pub-id-type="doi">10.1126/science.279.5359.2115</pub-id><pub-id pub-id-type="pmid">9516114</pub-id></citation>
</ref>
<ref id="B75">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Lukhtanov</surname> <given-names>V. A.</given-names></name> <name><surname>Kandul</surname> <given-names>N. P.</given-names></name> <name><surname>Plotkin</surname> <given-names>J. B.</given-names></name> <name><surname>Dantchenko</surname> <given-names>A. V.</given-names></name> <name><surname>Haig</surname> <given-names>D.</given-names></name> <name><surname>Pierce</surname> <given-names>N. E.</given-names></name></person-group> (<year>2005</year>). <article-title>Reinforcement of pre-zygotic isolation and karyotype evolution in Agrodiaetus butterflies</article-title>. <source>Nature</source> <volume>436</volume>, <fpage>385</fpage>&#x02013;<lpage>389</lpage>. <pub-id pub-id-type="doi">10.1038/nature03704</pub-id><pub-id pub-id-type="pmid">16034417</pub-id></citation>
</ref>
<ref id="B76">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>MacArthur</surname> <given-names>R. H.</given-names></name></person-group> (<year>1969</year>). <article-title>Patterns of communities in the tropics</article-title>. <source>Biol. J. Linnean Soc</source>. <volume>1</volume>, <fpage>19</fpage>&#x02013;<lpage>30</lpage>. <pub-id pub-id-type="doi">10.1111/j.1095-8312.1969.tb01809.x</pub-id></citation>
</ref>
<ref id="B77">
<citation citation-type="book"><person-group person-group-type="author"><name><surname>MacArthur</surname> <given-names>R. H.</given-names></name> <name><surname>Wilson</surname> <given-names>E. O.</given-names></name></person-group> (<year>1967</year>). <source>The Theory of Island Biogeography. Monographs in Population Biology</source>. <publisher-loc>New Jersey</publisher-loc>: <publisher-name>Princeton University Press</publisher-name>.</citation>
</ref>
<ref id="B78">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Martin</surname> <given-names>P. R.</given-names></name> <name><surname>McKay</surname> <given-names>J. K.</given-names></name></person-group> (<year>2004</year>). <article-title>Latitudinal variation in genetic divergence of populations and the potential for future speciation</article-title>. <source>Evolution</source> <volume>58</volume>, <fpage>938</fpage>&#x02013;<lpage>945</lpage>. <pub-id pub-id-type="doi">10.1111/j.0014-3820.2004.tb00428.x</pub-id><pub-id pub-id-type="pmid">15212375</pub-id></citation>
</ref>
<ref id="B79">
<citation citation-type="book"><person-group person-group-type="author"><name><surname>Mayr</surname> <given-names>E.</given-names></name></person-group> (<year>1963</year>). <source>Animal species and evolution</source>. <publisher-loc>Cambridge</publisher-loc>: <publisher-name>Harvard University Press</publisher-name>.</citation>
</ref>
<ref id="B80">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>McBride</surname> <given-names>C. S.</given-names></name> <name><surname>Singer</surname> <given-names>M. C.</given-names></name></person-group> (<year>2010</year>). <article-title>Field studies reveal strong postmating isolation between ecologically divergent butterfly populations</article-title>. <source>PLoS Biol</source>. <volume>8</volume>:<fpage>e1000529</fpage>. <pub-id pub-id-type="doi">10.1371/journal.pbio.1000529</pub-id><pub-id pub-id-type="pmid">21048982</pub-id></citation>
</ref>
<ref id="B81">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>McPeek</surname> <given-names>M. A.</given-names></name> <name><surname>Holt</surname> <given-names>R. D.</given-names></name></person-group> (<year>1992</year>). <article-title>The Evolution of dispersal in spatially and temporally varying environments</article-title>. <source>Am. Nat</source>. <volume>140</volume>, <fpage>1010</fpage>. <pub-id pub-id-type="doi">10.1086/285453</pub-id></citation>
</ref>
<ref id="B82">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Millien</surname> <given-names>V.</given-names></name></person-group> (<year>2006</year>). <article-title>Morphological evolution is accelerated among island mammals</article-title>. <source>PLoS Biol</source>. <volume>4</volume>:<fpage>e321</fpage>. <pub-id pub-id-type="doi">10.1371/journal.pbio.0040321</pub-id><pub-id pub-id-type="pmid">16968136</pub-id></citation>
</ref>
<ref id="B83">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Mittelbach</surname> <given-names>G. G.</given-names></name> <name><surname>Schemske</surname> <given-names>D. W.</given-names></name> <name><surname>Cornell</surname> <given-names>H. V.</given-names></name> <name><surname>Allen</surname> <given-names>A. P.</given-names></name> <name><surname>Brown</surname> <given-names>J. M.</given-names></name> <name><surname>Bush</surname> <given-names>M. B.</given-names></name> <etal/></person-group>. (<year>2007</year>). <article-title>Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography</article-title>. <source>Ecol. Lett</source>. <volume>10</volume>, <fpage>315</fpage>&#x02013;<lpage>331</lpage>. <pub-id pub-id-type="doi">10.1111/j.1461-0248.2007.01020.x</pub-id><pub-id pub-id-type="pmid">17355570</pub-id></citation>
</ref>
<ref id="B84">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Mona</surname> <given-names>S.</given-names></name> <name><surname>Ray</surname> <given-names>N.</given-names></name> <name><surname>Arenas</surname> <given-names>M.</given-names></name> <name><surname>Excoffier</surname> <given-names>L.</given-names></name></person-group> (<year>2014</year>). <article-title>Genetic consequences of habitat fragmentation during a range expansion</article-title>. <source>Heredity</source> <volume>112</volume>, <fpage>291</fpage>&#x02013;<lpage>299</lpage>. <pub-id pub-id-type="doi">10.1038/hdy.2013.105</pub-id><pub-id pub-id-type="pmid">24149654</pub-id></citation>
</ref>
<ref id="B85">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Ohta</surname> <given-names>T.</given-names></name></person-group> (<year>1992</year>). <article-title>The nearly neutral theory of molecular evolution</article-title>. <source>Annu. Rev. Ecol. Evol. Syst</source>. <volume>23</volume>, <fpage>263</fpage>&#x02013;<lpage>286</lpage>. <pub-id pub-id-type="doi">10.1146/annurev.es.23.110192.001403</pub-id></citation>
</ref>
<ref id="B86">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Ohta</surname> <given-names>T.</given-names></name></person-group> (<year>2002</year>). <article-title>Near-neutrality in evolution of genes and gene regulation</article-title>. <source>Proc. Natl. Acad. Sci. U.S.A</source>. <volume>99</volume>, <fpage>16134</fpage>&#x02013;<lpage>16137</lpage>. <pub-id pub-id-type="doi">10.1073/pnas.252626899</pub-id><pub-id pub-id-type="pmid">12461171</pub-id></citation>
</ref>
<ref id="B87">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Ozinga</surname> <given-names>W. A.</given-names></name> <name><surname>Bekker</surname> <given-names>R. M.</given-names></name> <name><surname>Schamin&#x000E9;e</surname> <given-names>J. H. J.</given-names></name> <name><surname>van Groenendael</surname> <given-names>J. M.</given-names></name></person-group> (<year>2004</year>). <article-title>Dispersal potential in plant communities depends on environmental conditions</article-title>. <source>J. Ecol</source>. <volume>92</volume>, <fpage>767</fpage>&#x02013;<lpage>777</lpage>. <pub-id pub-id-type="doi">10.1111/j.0022-0477.2004.00916.x</pub-id></citation>
</ref>
<ref id="B88">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Panero</surname> <given-names>J. L.</given-names></name> <name><surname>Francisco-Ortega</surname> <given-names>J.</given-names></name> <name><surname>Jansen</surname> <given-names>R. K.</given-names></name> <name><surname>Santos-Guerra</surname> <given-names>A.</given-names></name></person-group> (<year>1999</year>). <article-title>Molecular evidence for multiple origins of woodiness and a new world biogeographic connection of the Macaronesian island endemic Pericallis (Asteraceae: senecioneae)</article-title>. <source>Proc. Natl. Acad. Sci. U.S.A</source>. <volume>96</volume>, <fpage>13886</fpage>&#x02013;<lpage>13891</lpage>. <pub-id pub-id-type="doi">10.1073/pnas.96.24.13886</pub-id><pub-id pub-id-type="pmid">10570168</pub-id></citation>
</ref>
<ref id="B89">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Pellissier</surname> <given-names>L.</given-names></name> <name><surname>Leprieur</surname> <given-names>F.</given-names></name> <name><surname>Parravicini</surname> <given-names>V.</given-names></name> <name><surname>Cowman</surname> <given-names>P. F.</given-names></name> <name><surname>Kulbicki</surname> <given-names>M.</given-names></name> <name><surname>Litsios</surname> <given-names>G.</given-names></name> <etal/></person-group>. (<year>2014</year>). <article-title>Quaternary coral reef refugia preserved fish diversity</article-title>. <source>Science</source> <volume>344</volume>, <fpage>1016</fpage>&#x02013;<lpage>1019</lpage>. <pub-id pub-id-type="doi">10.1126/science.1249853</pub-id><pub-id pub-id-type="pmid">24876495</pub-id></citation>
</ref>
<ref id="B90">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Pellissier</surname> <given-names>L.</given-names></name> <name><surname>Litsios</surname> <given-names>G.</given-names></name> <name><surname>Guisan</surname> <given-names>A.</given-names></name> <name><surname>Alvarez</surname> <given-names>N.</given-names></name></person-group> (<year>2012</year>). <article-title>Molecular substitution rate increases in myrmecophilous lycaenid butterflies (Lepidoptera)</article-title>. <source>Zool. Scr</source>. <volume>41</volume>, <fpage>651</fpage>&#x02013;<lpage>658</lpage>. <pub-id pub-id-type="doi">10.1111/j.1463-6409.2012.00556.x</pub-id></citation>
</ref>
<ref id="B91">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Pierce</surname> <given-names>N. E.</given-names></name> <name><surname>Nash</surname> <given-names>D. R.</given-names></name></person-group> (<year>1999</year>). <article-title>The imperial blue, <italic>Jalmenus evagoras</italic> (Lycaenidae)</article-title>. <source>Monogr. Aust. Lepidoptera</source> <volume>6</volume>, <fpage>279</fpage>&#x02013;<lpage>315</lpage>.</citation>
</ref>
<ref id="B92">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Popadin</surname> <given-names>K.</given-names></name> <name><surname>Polishchuk</surname> <given-names>L. V.</given-names></name> <name><surname>Mamirova</surname> <given-names>L.</given-names></name> <name><surname>Knorre</surname> <given-names>D.</given-names></name> <name><surname>Gunbin</surname> <given-names>K.</given-names></name></person-group> (<year>2007</year>). <article-title>Accumulation of slightly deleterious mutations in mitochondrial protein-coding genes of large versus small mammals</article-title>. <source>Proc. Natl. Acad. Sci. U.S.A</source>. <volume>104</volume>, <fpage>13390</fpage>&#x02013;<lpage>13395</lpage>. <pub-id pub-id-type="doi">10.1073/pnas.0701256104</pub-id><pub-id pub-id-type="pmid">17679693</pub-id></citation>
</ref>
<ref id="B93">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Ramsey</surname> <given-names>J.</given-names></name> <name><surname>Bradshaw</surname> <given-names>H. D.</given-names></name> <name><surname>Schemske</surname> <given-names>D. W.</given-names></name></person-group> (<year>2003</year>). <article-title>Components of reproductive isolation between the monkeyflowers <italic>Mimulus lewisii</italic> and <italic>M. cardinalis</italic> (Phrymaceae)</article-title>. <source>Evolution</source> <volume>57</volume>, <fpage>1520</fpage>&#x02013;<lpage>1534</lpage>. <pub-id pub-id-type="doi">10.1111/j.0014-3820.2003.tb00360.x</pub-id><pub-id pub-id-type="pmid">12940357</pub-id></citation>
</ref>
<ref id="B94">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Riginos</surname> <given-names>C.</given-names></name> <name><surname>Buckley</surname> <given-names>Y.</given-names></name> <name><surname>Blomber</surname> <given-names>S. P.</given-names></name> <name><surname>Treml</surname> <given-names>E. A.</given-names></name></person-group> (<year>2014</year>). <article-title>Dispersal capacity predicts both population genetic structure and species richness in reef fishes</article-title>. <source>Am. Nat</source>. <volume>184</volume>, <fpage>52</fpage>&#x02013;<lpage>64</lpage> <pub-id pub-id-type="doi">10.1086/676505</pub-id><pub-id pub-id-type="pmid">24921600</pub-id></citation>
</ref>
<ref id="B95">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Rohde</surname> <given-names>K.</given-names></name></person-group> (<year>2007</year>). <article-title>Latitudinal gradients in species diversity?: the search for the primary cause</article-title>. <source>Oikos</source> <volume>65</volume>, <fpage>514</fpage>&#x02013;<lpage>527</lpage>. <pub-id pub-id-type="doi">10.2307/3545569</pub-id></citation>
</ref>
<ref id="B96">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Romiguier</surname> <given-names>J.</given-names></name> <name><surname>Gayral</surname> <given-names>P.</given-names></name> <name><surname>Ballenghien</surname> <given-names>M.</given-names></name> <name><surname>Bernard</surname> <given-names>A.</given-names></name> <name><surname>Cahais</surname> <given-names>V.</given-names></name> <name><surname>Chenuil</surname> <given-names>A.</given-names></name> <etal/></person-group>. (<year>2014</year>). <article-title>Comparative population genomics in animals uncovers the determinants of genetic diversity</article-title>. <source>Nature</source> <volume>515</volume>, <fpage>261</fpage>&#x02013;<lpage>263</lpage>. <pub-id pub-id-type="doi">10.1038/nature13685</pub-id><pub-id pub-id-type="pmid">25141177</pub-id></citation>
</ref>
<ref id="B97">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Roxburgh</surname> <given-names>S. H.</given-names></name> <name><surname>Shea</surname> <given-names>K.</given-names></name> <name><surname>Wilson</surname> <given-names>J. B.</given-names></name></person-group> (<year>2004</year>). <article-title>The intermediate disturbance hypothesis: patch dynamics and mechanisms of species coexistence</article-title>. <source>Ecology</source> <volume>85</volume>, <fpage>359</fpage>&#x02013;<lpage>371</lpage>. <pub-id pub-id-type="doi">10.1890/03-0266</pub-id><pub-id pub-id-type="pmid">16875700</pub-id></citation>
</ref>
<ref id="B98">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Salisbury</surname> <given-names>C. L.</given-names></name> <name><surname>Seddon</surname> <given-names>N.</given-names></name> <name><surname>Cooney</surname> <given-names>C. R.</given-names></name> <name><surname>Tobias</surname> <given-names>J. A.</given-names></name></person-group> (<year>2012</year>). <article-title>The latitudinal gradient in dispersal constraints: ecological specialisation drives diversification in tropical birds</article-title>. <source>Ecol. Lett</source>. <volume>15</volume>, <fpage>847</fpage>&#x02013;<lpage>855</lpage>. <pub-id pub-id-type="doi">10.1111/j.1461-0248.2012.01806.x</pub-id><pub-id pub-id-type="pmid">22639858</pub-id></citation>
</ref>
<ref id="B99">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Schemske</surname> <given-names>D. W.</given-names></name> <name><surname>Mittelbach</surname> <given-names>G. G.</given-names></name> <name><surname>Cornell</surname> <given-names>H. V.</given-names></name> <name><surname>Sobel</surname> <given-names>J. M.</given-names></name> <name><surname>Roy</surname> <given-names>K.</given-names></name></person-group> (<year>2009</year>). <article-title>Is there a latitudinal gradient in the importance of biotic interactions?</article-title> <source>Annu. Rev. Ecol. Evol. Syst</source>. <volume>40</volume>, <fpage>245</fpage>&#x02013;<lpage>269</lpage>. <pub-id pub-id-type="doi">10.1146/annurev.ecolsys.39.110707.173430</pub-id></citation>
</ref>
<ref id="B100">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Schliewen</surname> <given-names>U. K.</given-names></name> <name><surname>Tautz</surname> <given-names>D.</given-names></name> <name><surname>P&#x000E4;&#x000E4;bo</surname> <given-names>S.</given-names></name></person-group> (<year>1994</year>). <article-title>Sympatric speciation suggested by monophyly of crater lake cichlids</article-title>. <source>Nature</source> <volume>368</volume>, <fpage>629</fpage>&#x02013;<lpage>632</lpage>. <pub-id pub-id-type="doi">10.1038/368629a0</pub-id><pub-id pub-id-type="pmid">8145848</pub-id></citation>
</ref>
<ref id="B101">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Schluter</surname> <given-names>D.</given-names></name></person-group> (<year>2000</year>). <article-title>Ecological character displacement in adaptive radiation</article-title>. <source>Am. Nat</source>. <volume>156</volume>, <fpage>S4</fpage>&#x02013;<lpage>S16</lpage>. <pub-id pub-id-type="doi">10.1086/303412</pub-id></citation>
</ref>
<ref id="B102">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Schluter</surname> <given-names>D.</given-names></name></person-group> (<year>2009</year>). <article-title>Evidence for ecological speciation and its alternative</article-title>. <source>Science</source> <volume>323</volume>, <fpage>737</fpage>&#x02013;<lpage>741</lpage>. <pub-id pub-id-type="doi">10.1126/science.1160006</pub-id><pub-id pub-id-type="pmid">19197053</pub-id></citation>
</ref>
<ref id="B103">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Smith</surname> <given-names>M. A.</given-names></name> <name><surname>Rodriguez</surname> <given-names>J. J.</given-names></name> <name><surname>Whitfield</surname> <given-names>J. B.</given-names></name> <name><surname>Deans</surname> <given-names>A. R.</given-names></name> <name><surname>Janzen</surname> <given-names>D. H.</given-names></name> <name><surname>Hallwachs</surname> <given-names>W.</given-names></name> <etal/></person-group>. (<year>2008</year>). <article-title>Extreme diversity of tropical parasitoid wasps exposed by iterative integration of natural history, DNA barcoding, morphology, and collections</article-title>. <source>Proc. Natl. Acad. Sci. U.S.A</source>. <volume>105</volume>, <fpage>12359</fpage>&#x02013;<lpage>12364</lpage>. <pub-id pub-id-type="doi">10.1073/pnas.0805319105</pub-id><pub-id pub-id-type="pmid">18716001</pub-id></citation>
</ref>
<ref id="B104">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Stegen</surname> <given-names>J. C.</given-names></name> <name><surname>Enquist</surname> <given-names>B. J.</given-names></name> <name><surname>Ferriere</surname> <given-names>R.</given-names></name></person-group> (<year>2009</year>). <article-title>Advancing the metabolic theory of biodiversity</article-title>. <source>Ecol. Lett</source>. <volume>12</volume>, <fpage>1001</fpage>&#x02013;<lpage>1015</lpage>. <pub-id pub-id-type="doi">10.1111/j.1461-0248.2009.01358.x</pub-id><pub-id pub-id-type="pmid">19747180</pub-id></citation>
</ref>
<ref id="B105">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Stevens</surname> <given-names>G. C.</given-names></name></person-group> (<year>1989</year>). <article-title>The latitudinal gradient in geographical range: how so many species coexist in the tropics</article-title>. <source>Am. Nat</source>. <volume>133</volume>, <fpage>240</fpage>&#x02013;<lpage>256</lpage>. <pub-id pub-id-type="doi">10.1086/284913</pub-id></citation>
</ref>
<ref id="B106">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Surget-Groba</surname> <given-names>Y.</given-names></name> <name><surname>Kay</surname> <given-names>K. M.</given-names></name></person-group> (<year>2013</year>). <article-title>Restricted gene flow within and between rapidly diverging Neotropical plant species</article-title>. <source>Mol. Ecol</source>. <volume>22</volume>, <fpage>4931</fpage>&#x02013;<lpage>4942</lpage>. <pub-id pub-id-type="doi">10.1111/mec.12442</pub-id><pub-id pub-id-type="pmid">23952304</pub-id></citation>
</ref>
<ref id="B107">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Tachida</surname> <given-names>H.</given-names></name> <name><surname>Iizuka</surname> <given-names>M.</given-names></name></person-group> (<year>1991</year>). <article-title>Fixation probability in spatially changing environments</article-title>. <source>Genet. Res</source>. <volume>58</volume>, <fpage>243</fpage>&#x02013;<lpage>251</lpage>. <pub-id pub-id-type="doi">10.1017/S0016672300029992</pub-id><pub-id pub-id-type="pmid">1802806</pub-id></citation>
</ref>
<ref id="B108">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Theim</surname> <given-names>T. J.</given-names></name> <name><surname>Shirk</surname> <given-names>R. Y.</given-names></name> <name><surname>Givnish</surname> <given-names>T. J.</given-names></name></person-group> (<year>2014</year>). <article-title>Spatial genetic structure in four understory Psychotria species (Rubiaceae) and implications for tropical forest diversity</article-title>. <source>Am. J. Bot</source>. <volume>101</volume>, <fpage>1189</fpage>&#x02013;<lpage>1199</lpage>. <pub-id pub-id-type="doi">10.3732/ajb.1300460</pub-id><pub-id pub-id-type="pmid">25002460</pub-id></citation>
</ref>
<ref id="B109">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Tilman</surname> <given-names>D.</given-names></name></person-group> (<year>1985</year>). <article-title>The resource-ratio hypothesis of plant succession</article-title>. <source>Am. Nat</source>. <volume>125</volume>, <fpage>827</fpage>. <pub-id pub-id-type="doi">10.1086/284382</pub-id></citation>
</ref>
<ref id="B110">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Turnbull</surname> <given-names>L.</given-names></name> <name><surname>Turnbull</surname> <given-names>L.</given-names></name> <name><surname>Rees</surname> <given-names>M.</given-names></name> <name><surname>Rees</surname> <given-names>M.</given-names></name> <name><surname>Crawley</surname> <given-names>M. J.</given-names></name> <name><surname>Crawley</surname> <given-names>M. J.</given-names></name></person-group> (<year>1999</year>). <article-title>Seed mass and the competition/colonization trade-of: a sowing experiment</article-title>. <source>J. Ecol</source>. <volume>87</volume>, <fpage>899</fpage>&#x02013;<lpage>912</lpage>. <pub-id pub-id-type="doi">10.1046/j.1365-2745.1999.00405.x</pub-id></citation>
</ref>
<ref id="B111">
<citation citation-type="book"><person-group person-group-type="author"><name><surname>Wallace</surname> <given-names>A. R.</given-names></name></person-group> (<year>1878</year>). <source>Tropical Nature and other Essays</source>. <publisher-loc>New York, NY</publisher-loc>: <publisher-name>Macmillan</publisher-name>.</citation>
</ref>
<ref id="B112">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Weber</surname> <given-names>C. C.</given-names></name> <name><surname>Nabholz</surname> <given-names>B.</given-names></name> <name><surname>Romiguier</surname> <given-names>J.</given-names></name> <name><surname>Ellegren</surname> <given-names>H.</given-names></name></person-group> (<year>2014</year>). <article-title>Kr/Kc but not dN/dS correlates positively with body mass in birds, raising implications for inferring lineage-specific selection</article-title>. <source>Genome Biol</source>. <volume>15</volume>:<fpage>542</fpage>. <pub-id pub-id-type="doi">10.1186/s13059-014-0542-8</pub-id><pub-id pub-id-type="pmid">25607475</pub-id></citation>
</ref>
<ref id="B113">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Weir</surname> <given-names>J. T.</given-names></name> <name><surname>Schluter</surname> <given-names>D.</given-names></name></person-group> (<year>2007</year>). <article-title>The latitudinal gradient in recent speciation and extinction rates of birds and mammals</article-title>. <source>Science</source> <volume>315</volume>, <fpage>1574</fpage>&#x02013;<lpage>1576</lpage>. <pub-id pub-id-type="doi">10.1126/science.1135590</pub-id><pub-id pub-id-type="pmid">17363673</pub-id></citation>
</ref>
<ref id="B114">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>White</surname> <given-names>G. M.</given-names></name> <name><surname>Boshier</surname> <given-names>D. H.</given-names></name> <name><surname>Powell</surname> <given-names>W.</given-names></name></person-group> (<year>2002</year>). <article-title>Increased pollen flow counteracts fragmentation in a tropical dry forest: an example from <italic>Swietenia humilis</italic> Zuccarini</article-title>. <source>Proc. Natl. Acad. Sci. U.S.A</source>. <volume>99</volume>, <fpage>2038</fpage>&#x02013;<lpage>2042</lpage>. <pub-id pub-id-type="doi">10.1073/pnas.042649999</pub-id><pub-id pub-id-type="pmid">11842203</pub-id></citation>
</ref>
<ref id="B115">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Wiens</surname> <given-names>J. J.</given-names></name> <name><surname>Donoghue</surname> <given-names>M. J.</given-names></name></person-group> (<year>2004</year>). <article-title>Historical biogeography, ecology and species richness</article-title>. <source>Trends Ecol. Evol</source>. <volume>19</volume>, <fpage>639</fpage>&#x02013;<lpage>644</lpage>. <pub-id pub-id-type="doi">10.1016/j.tree.2004.09.011</pub-id><pub-id pub-id-type="pmid">16701326</pub-id></citation>
</ref>
<ref id="B116">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Williams</surname> <given-names>S. E.</given-names></name> <name><surname>Williams</surname> <given-names>Y. M.</given-names></name> <name><surname>VanDerWal</surname> <given-names>J.</given-names></name> <name><surname>Isaac</surname> <given-names>J. L.</given-names></name> <name><surname>Shoo</surname> <given-names>L. P.</given-names></name> <name><surname>Johnson</surname> <given-names>C. N.</given-names></name></person-group> (<year>2009</year>). <article-title>Ecological specialization and population size in a biodiversity hotspot: how rare species avoid extinction</article-title>. <source>Proc. Natl. Acad. Sci. U.S.A</source>. <volume>106(Suppl. 2)</volume>, <fpage>19737</fpage>&#x02013;<lpage>19741</lpage>. <pub-id pub-id-type="doi">10.1073/pnas.0901640106</pub-id><pub-id pub-id-type="pmid">19897718</pub-id></citation>
</ref>
<ref id="B117">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Woolfit</surname> <given-names>M.</given-names></name> <name><surname>Bromham</surname> <given-names>L.</given-names></name></person-group> (<year>2005</year>). <article-title>Population size and molecular evolution on islands</article-title>. <source>Proc. Biol. Sci</source>. <volume>272</volume>, <fpage>2277</fpage>&#x02013;<lpage>2282</lpage>. <pub-id pub-id-type="doi">10.1098/rspb.2005.3217</pub-id><pub-id pub-id-type="pmid">16191640</pub-id></citation>
</ref>
<ref id="B118">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Wright</surname> <given-names>S.</given-names></name></person-group> (<year>1946</year>). <article-title>Isolation by distance under diverse systems of mating</article-title>. <source>Genetics</source> <volume>31</volume>, <fpage>39</fpage>&#x02013;<lpage>59</lpage>. <pub-id pub-id-type="pmid">21009706</pub-id></citation>
</ref>
<ref id="B119">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Wright</surname> <given-names>S.</given-names></name> <name><surname>Keeling</surname> <given-names>J.</given-names></name> <name><surname>Gillman</surname> <given-names>L.</given-names></name></person-group> (<year>2006</year>). <article-title>The road from Santa Rosalia: a faster tempo of evolution in tropical climates</article-title>. <source>Proc. Natl. Acad. Sci. U.S.A</source>. <volume>103</volume>, <fpage>7718</fpage>&#x02013;<lpage>7722</lpage>. <pub-id pub-id-type="doi">10.1073/pnas.0510383103</pub-id><pub-id pub-id-type="pmid">16672371</pub-id></citation>
</ref>
<ref id="B120">
<citation citation-type="journal"><person-group person-group-type="author"><name><surname>Zayed</surname> <given-names>A.</given-names></name> <name><surname>Packer</surname> <given-names>L.</given-names></name></person-group> (<year>2007</year>). <article-title>The population genetics of a solitary oligolectic sweat bee, Lasioglossum (Sphecodogastra) oenotherae (Hymenoptera: Halictidae)</article-title>. <source>Heredity</source> <volume>99</volume>, <fpage>397</fpage>&#x02013;<lpage>405</lpage>. <pub-id pub-id-type="doi">10.1038/sj.hdy.6801013</pub-id><pub-id pub-id-type="pmid">17534381</pub-id></citation>
</ref>
</ref-list>
</back>
</article>