The rise of phylogenetic systematics (Hennig, 1950) uncovered many natural groups of amniotes with Synapsida-characterized by one temporal opening, and Reptilia (Modesto and Anderson, 2004)-which contains ancestral, typically anapsid groups, without temporal openings, and Diapsida, with two temporal openings and diverse secondary modifications. The ancestrally anapsid parareptiles partly show, with certain ontogenetic, inter-, and intra-specific variation, one opening or marginal excavation in their temporal region (Cisneros et al., 2004; Tsuji and Müller, 2009; MacDougall and Reisz, 2014), although evidence from other characters clearly separates them from Synapsida (Müller, 2004; Tsuji et al., 2012; Brocklehurst et al., 2018). Furthermore, the phylogenetic position of one early “classical” synapsid group (i.e., varanopsids) has become controversial, as it has appeared within Reptilia in some phylogenetic analyses (Ford and Benson, 2018; Laurin and Piñeiro, 2018). Compared to historical classifications (Osborn, 1903; Williston, 1917; Goodrich, 1930), there is a common consensus that temporal openings are only a weak indication for higher taxon interrelationship, although it can be informative on lower taxonomic level (Müller, 2003; Laurin and Piñeiro, 2018; MacDougall et al., 2018). Here, I present a rather morphofunctional categorization of temporal openings, introduce a refined terminology, and provide an ontogenetic explanation on their evolutionary origins.
Morphofunctional Categorization
I) Anapsid
The ancestral amniote skull likely had an anapsid shape comparable to the skull of non-amniote groups such as the lungfish with full temporal coverage. Jaw muscles broadly originated from the internal surface of the dermatocranial bones of the temporal region and inserted on the lower jaw (Figure 1I, B, B′, C).
Figure 1
II) Monapsid
When compared to early anapsid tetrapods, temporal openings in amniotes are correlated to higher domed skulls, which provide space for longer, more voluminous, and hence stronger jaw muscles. Partly via tendons, jaw musculature originates mainly from the edges of an opening, which, due to its round shape, provides a greater structural stability than a flat bone (Case, 1924; Frazzetta, 1968; Tarsitano et al., 2001; Werneburg, 2013a). In that way, a different bite performance can be reached on shore. Early fossil Synapsida were predators and herbivores and their temporal opening might have supported the progressing development of stronger jaw musculature for biting (Figure 1-II) (Kemp, 2005; Angielczyck and Kammerer, 2018). Adaptive radiation, later on, resulted in the secondary evolution of diverse feeding modes, correlated to tooth morphology, for example, illustrating that the morphofunctional category of a temporal opening is not a general proxy for feeding ecology.
Monapsid skulls can also appear in parareptilians and the fenestra can be formed between different bones (Tsuji and Müller, 2009; MacDougall and Reisz, 2014; Laurin and Piñeiro, 2017). The variable position and shape of the fenestra in different parareptilian taxa suggests diverse jaw muscle attachments and bite performances in that group, which included herbivores, carnivores, and insectivors. In many cases, it is not certain whether a “skull hole” is a taphonomic artifact or a real temporal opening (Brocklehurst et al., 2018).
III) Diplapsid
Diapsida usually have broader skull roofs (Weishampel et al., 2004), which permits an upper temporal fenestra to develop (Figure 1-III) (Tarsitano et al., 2001). Whether a second, lower temporal opening is ancestral for Diapsida is debated (Evans, 2008), but likely (Figure 1-8). When that bar is not present, the skull is called katapsid (Figure 1-9).
Different to the carnivorous and herbivorous early Synapsida, early Diapsida were certainly insectivorous and had to handle the agile food. For that, the edges of two temporal openings (diplapsid condition; I avoid the term ‘diapsid’ for this morphotype to prevent confusion with the taxon Diapsida - similar to ‘synapsid’/Synapsida) provided complex attachment sites for a highly differentiated jaw musculature permitting very flexible movements of the jaw apparatus (Holliday and Witmer, 2007; Evans, 2008; Daza et al., 2011). Later in evolution, also other feeding modes evolved within Diapsida, partly associated to comprehensive cranial kinesis (Figure 1-9, 10, 16).
IV) Excavation
To increase force with longer fibers and to develop more diverse attachment sites, musculature can expand beyond the restrictions of the ancestral temporal anatomy resulting in deep embayments in the dermal skeleton and/or the loss of temporal arcades (Figure 1-IV). Those excavations are known as (a) emarginations, marginal reductions of bones at the edge of the whole temporal region, as well as (b) internal expansions of the temporal fenestrae themselves. Different combinations and degrees of excavations exist, like all morphofunctional categories presented herein are usually fluent.
In different clades of Synapsida, the temporal opening increased in size (Figure 1-21). By suppressing the ancestral posttemporal opening in the occipital region and partly the postorbital bar, the temporalis muscle expands through the temporal fenestra, extends to the external surface of the skull roof and, with that, develops longer muscle fibers to increase bite force. The zygomatic arch serves as origin site for the newly differentiated masseter muscle, enabling chewing along the mammalian stem and leaving an emargination in the arch (Figure 1-21) (Abdala and Damiani, 2004; Werneburg, 2013a; Lautenschlager et al., 2016).
Similar evolutionary patterns can be recognized in some extinct marine reptiles (Figure 1-13, 14), for example, in which the upper temporal opening expands in diameter and even a dorsal parietal crest for the origin of jaw musculature can be developed (Rieppel, 2002), like in several groups of Synapsida. High predatory behavior in the diapsid marine ichthyosaurs and sauropterygians (Liu et al., 2017) might have triggered the dorsal expansion of the jaw musculature and hence the expansion of the upper temporal opening resulting in the secondary modification (i.e., closure and/or emargination) of the lower temporal region as well (Rieppel, 2002). Associated to expanding and hence stronger jaw musculature, a stiffening of the originally kinetic skull toward an akinetic morphology can be recognized (e.g., reduction of basicranial articulation, formation of a secondary braincase wall) (Werneburg et al., 2019).
There is growing consensus that turtles are derived from diapsid (Figure 1-17) reptiles (Rieppel, 2008; Wang et al., 2013; Schoch and Sues, 2015). Neck retraction in stem turtles certainly resulted in the closure of the ancestral temporal opening(s) to resist with a more compact, anapsid skull the tension of the neck musculature in the occipital region (Werneburg, 2015; Werneburg et al., 2015a,b). This novel skull anatomy, consequently, differs from the anapsid skull bone configurations of early Reptilia (Müller, 2003). Crown turtles evolved longer necks and highly elaborated neck retraction modes (Herrel et al., 2008). To resist the resulting increased neck tension, reductions were introduced to the margins of the temporal region, as they provide broader neck-muscle attachment sites that enable better force distribution (Figure 1-18) (Werneburg, 2012, 2015). The posterodorsal emargination, an excavation of the ancestral posttemporal (occipital) fenestra, finally enabled the jaw musculature to expand. This muscle expansion was necessary to bend around the large otic region in modern turtles, which restricts the space inside the adductor chamber (Rieppel, 1990; Werneburg, 2013b; Ferreira and Werneburg, 2019). As a result, although longer, jaw musculature is - different to mammals - more narrow and relatively less powerful. As such, it might not trigger the reduction of cranial kinesis in that way (Herrel et al., 2002). Nevertheless, skull stiffening takes place in the turtle stem already (Sterli and De La Fuente, 2010) to resist embryonic neck muscle activity (Werneburg and Maier, 2019).
Large marginal excavations are not only present in Diapsida or Synapsida. They can even be formed within anapsidian parareptiles, including orbital expansions (Figure 1-6, 7).
The temporal openings in diapsids experienced numerous modifications including the reduction or closure of the lower temporal opening (Figure 1-9, 10, 13, 14) (Rieppel and Gronowski, 1981; Reisz et al., 1984), a fusion of both openings with the reduction of the temporal arcades (Figure 1-12) (Cundall and Irish, 2008), and a fusion of both openings with the expanded orbita (Figure 1-16) (Zusi, 1993). Almost all amniotes, including Diapsida, evolved highly diverse feeding modes, ranging from insectivory and herbivory to piscivory and carnivory, from biting and chewing to filter and suction feeding, among others (Schwenk, 2000; Silva et al., 2017). This illustrates the general and extraordinary functional plasticity of the temporal skull anatomy in amniotes (Müller, 2003), which breaks phylogenetic constrains and opens avenues for the evolution of new skull shapes (Werneburg et al., 2019). To understand diversity of the temporal region, phylogeny appears to be less useful than studies of functional adaptations.
Ontogenetic Plasticity
The obviously non-exhaustive and simplified functional categorization of temporal fenestrations presented herein only concerns the more proximate explanations of phylogenetically young functional adaptatations. The ultimate causation in the sense of deep time evolutionary change, however, might be detected in life history changes (Sánchez-Villagra, 2012). The majority of non-amniote vertebrates has an anapsid morphotype. Exceptions are chondrichthyans, which lost their dermatocranium completely (Kardong, 2008), some microsaurian lepospondyls (Gee et al., 2019), and batrachian lissamphibians, which, by flattening of their ancestor's skull, largely rearranged their jaw musculature and skull architecture (Rieppel, 1981; Schoch, 2014). The new muscle arrangements in batrachians correlate with the loss of ossification centers through ontogeny as those are no longer recruited as attachment sites through development. This eventually resulted in the complete loss of several “non-used” temporal skull bones in the adults (Schoch, 2014).
Amniotes are characterized by the amniotic egg, which enables complete development of the animal outside an aquatic environment and consequently the invasion of different terrestrial habitats (Sumida and Martin, 1997; Laurin, 2010; Skawiski and Tałanda, 2014; Brocklehurst et al., 2018). With development inside the egg [or, secondarily, inside the mother's womb (Piñeiro et al., 2012a; Werneburg et al., 2016)], the larval stage is lost and more or less fully formed, adult-resembling hatchings leave the eggs (Figure 1C). This is not the case in most extant non-amniotes, in which larvae hatch and have to feed (Figure 1A). For that, jaw (and branchial) musculature inserts primarily to the embryonic neurocranium (chondrocranium), as dermatocranial bones are not yet well-developed (Figure 1A′, A″) (Edgeworth, 1935; De Beer, 1937; Ziermann et al., 2018). As such, compared to amniotes, the primordial cartilaginous skull is highly functional. Dermatocranial and temporal skull bones are later influenced developmentally by the functional jaw musculature near the neurocranium and are incorporated to the feeding apparatus as further attachment sites (Figure 1A″, B′) (Ziermann et al., 2018). Furthermore, in non-tetrapods, opercle bones also contribute to the dermatocranial armor to protect gill arches, to regulate gill ventilation, and to form a natural and broad edge of the temporal region (Figure 1A′: dotted line) (Goodrich, 1930; De Beer, 1937; Kemp, 1999). Temporal bones “just” fill the narrow “gap“ between opercle bones and the skull roof.
Also water pressure on the skull in larvae and, if aquatic, in adults might result in the formation of a fully encapsulated skull in non-amniotes (Figure 1A, B) as is indicated by the extant amniotic marine turtles (Figure 1-19). Mesozoic marine turtles such as Toxochelys showed a typical turtle-emargination of the temporal region (Matzke, 2009) related to neck retraction. With the reduced ability of neck retraction and a shorter neck in crown marine turtles, a secondary closure of the temporal armor might also correspond to water pressure (Zdansky, 1923; Werneburg, 2012), a factor not present in pure terrestrial amniotes.
By skipping the larval stage (Figure 1C), the amniote's skull architecture and growth rate differs. The chondrocranium of amniotes becomes less functional for feeding, is hence anatomically more conserved, and the pharyngeal arches are highly modified (De Beer, 1937). The bones not spatially arranged by musculature in early development result in “the embryological failure to close sutures” (Tarsitano et al., 2001). Jaw musculature receives more freedom to diversify and to evolve in response to different feeding requirements as it is non-functional for a long period of development until hatching/birth. Depending on functional demands, just recently developed temporal bones [still losely “floating” on the head's surface (Figure 1C′)] are recruited by the specialized jaw musculature in ontogeny and are spatially arranged to become the newly required attachment sites (Figure 1C″) (Rieppel, 1987; Fucik, 1991). In that way, generally, apomorphic skull bone mosaics can be explained and, more specifically, the diverse shapes of temporal skull openings can be best interpreted by the functional (future) demands of the developing musculature. As correctly pointed out by the above-mentioned phylogenetic observations, temporal fenestrations between synapsids, parareptiles, and diapsids cannot be homologized (only tissue can): the “holes” in the dermatocranium are just the result of developmental plasticity driven by functional adaptations, which, again and finally, can only be informative on certain taxonomic levels.
At the dawn of amniote evolution, new habitats were invaded and new ecological adaptations were necessary (Sumida and Martin, 1997; Brocklehurst et al., 2018). The great diversity and plasticity of the temporal region of the skull in early amniote taxa of the Permian and Triassic, such as in parareptiles (Figure 1-4, 5, 6, 7) (Colbert, 1946; Tsuji et al., 2012; MacDougall and Reisz, 2014; Laurin and Piñeiro, 2017), illustrates the rapid adaptive radiation of vertebrates on land (Nuñez Demarco et al., 2018). The monapsid morphotype stabilized in Synapsida (Figure 1-20, 21), whereas an upper temporal opening stabilized in Diapsida (Figure 1-8), although secondary modifications occurred. These are driven by internal and external forces acting on the skull (Gregory and Adams, 1915) as best observable in turtle evolution.
Statements
Author contributions
The author confirms being the sole contributor of this work and has approved it for publication.
Funding
SNF-grant P300PA_164720, DFG-grant WE5440/6-1. The publication costs were mainly covered by the DFG-financed Open Access Publishing Funds of Universität Tübingen and by Leibniz Association.
Acknowledgments
This article is dedicated to Sören Werneburg. I thank Michel Laurin and Graciela H. Piñeiro for the invitation to write this short opinion piece. In addition to them, I thank Fernando Abdala, Robert R. Reisz, and Juan Carlos Cisneros for very useful and controverse comments on the manuscript. Moreover, I thank Oleksandr Yaryhin and Wolfgang Maier for discussion.
Conflict of interest
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.
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Summary
Keywords
fenestration, emargination, amniote cranial evolution, amniote embryos, musculature
Citation
Werneburg I (2019) Morphofunctional Categories and Ontogenetic Origin of Temporal Skull Openings in Amniotes. Front. Earth Sci. 7:13. doi: 10.3389/feart.2019.00013
Received
17 December 2018
Accepted
28 January 2019
Published
19 March 2019
Volume
7 - 2019
Edited by
Michel Laurin, UMR7207 Centre de Recherche sur la Paléobiodiversité et les Paléoenvironnements (CR2P), France
Reviewed by
Juan Carlos Cisneros, Federal University of Piauí, Brazil; Graciela Helena Piñeiro, Universidad de la República, Uruguay; Fernando Abdala, University of the Witwatersrand, South Africa
Updates
Copyright
© 2019 Werneburg.
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) and the copyright owner(s) 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.
*Correspondence: Ingmar Werneburg ingmar.werneburg@senckenberg.de
This article was submitted to Paleontology, a section of the journal Frontiers in Earth Science
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