Abstract
Studies across vertebrates have revealed significant insights into the processes that drive craniofacial morphogenesis, yet we still know little about how distinct facial morphologies are patterned during development. Studies largely point to evolution in GRNs of cranial progenitor cell types such as neural crest cells, as the major driver underlying adaptive cranial shapes. However, this hypothesis requires further validation, particularly within suitable models amenable to manipulation. By utilizing comparative models between related species, we can begin to disentangle complex developmental systems and identify the origin of species-specific patterning. Mammals present excellent evolutionary examples to scrutinize how these differences arise, as sister clades of eutherians and marsupials possess suitable divergence times, conserved cranial anatomies, modular evolutionary patterns, and distinct developmental heterochrony in their NCC behaviours and craniofacial patterning. In this review, I lend perspectives into the current state of mammalian craniofacial biology and discuss the importance of establishing a new marsupial model, the fat-tailed dunnart, for comparative research. Through detailed comparisons with the mouse, we can begin to decipher mammalian conserved, and species-specific processes and their contribution to craniofacial patterning and shape disparity. Recent advances in single-cell multi-omics allow high-resolution investigations into the cellular and molecular basis of key developmental processes. As such, I discuss how comparative evolutionary application of these tools can provide detailed insights into complex cellular behaviours and expression dynamics underlying adaptive craniofacial evolution. Though in its infancy, the field of “comparative evo-devo-omics” presents unparalleled opportunities to precisely uncover how phenotypic differences arise during development.
1 Introduction
One of the most remarkable, yet enigmatic aspects of the vertebrate skull is the broad diversity of craniofacial shapes observed between species. While our understanding of craniofacial biology has been significantly enhanced through investigations across several vertebrate models, we still know very little about the processes that drive the development of distinct craniofacial adaptations. Comparative embryology and developmental biology in jawed and jawless vertebrates have revealed that craniofacial morphogenesis is driven by a transient population of embryonic progenitors called the neural crest (; ). Multipotent neural crest cells (NCCs) direct patterning and development of the head and neck, amongst other structures, and are controlled by deeply conserved gene regulatory networks (GRNs) constituting a species-generic program (; ). The combination of these developmental and evolutionary observations, with forward genetics and human clinical models of craniofacial disease, have provided a holistic understanding of how the craniofacial prominences are patterned and skull bones develop (; ; ). However, despite this fundamental understanding of craniofacial biology across vertebrates, we still know remarkably little about how species-specific diversity arises and is patterned during development.
One way we can begin to address this phenomenon is by utilizing comparative models to quantitatively examine how disparities or similarities arise during development. These models need to be suitably chosen depending on the hypothesis being tested. i.e., examining closely related species with unique skull morphologies (disparity), versus distantly related species with similar skull morphologies (convergence). Mammals provide excellent examples to address these hypotheses, owing to their conserved anatomy yet remarkable craniofacial disparity or convergence, shared developmental patterns, heterochrony and lineage-specific constraints, and appropriate divergence times, e.g., within orders or across clades. Through application of these models, we can begin to tease apart how facial morphogenesis and shape diversity is regulated at the cellular and molecular level (; ; ), informing new models of development.
In this article, I outline my perspectives on establishing new comparative mammalian models for investigations into the developmental basis of craniofacial patterning. I discuss the underlying biology of craniofacial morphogenesis, including NCC biology, its influence on patterning, and heterochrony between therian mammals. I emphasize the importance of establishing an appropriate marsupial model for comparative investigations with the eutherian laboratory mouse, including the establishment and utilization of transgenic approaches. Finally, I discuss how single-cell multi-omic approaches, regularly utilized in developmental biology, should be applied to comparative craniofacial models to scrutinize differential cell and molecular behaviours underlying mammalian craniofacial patterning and shape diversity. Establishing a marsupial model for comparative mammalian biology will strengthen our understanding of craniofacial development and how morphological diversity is generated throughout evolution.
2 Neural Crest Cells and Patterning of the Head
Development of the vertebrate head and craniofacial skeleton is achieved largely through the contribution of migratory NCCs. NCC specification is regulated through a deeply-conserved GRN comprised of shared suites of core transcriptional regulators, constituting a species-generic program (; ). During early embryogenesis, NCCs arise within the neuroectoderm at the neural plate border (Figure 1A). Initially, WNT, FGF, and BMP signalling pathways define the border and initiate pre-migratory NCC specification in response to activation of SOX9 (). Committed NCCs undergo activation of epithelial-to-mesenchymal transcription factors, SOX10, SNAIL and SLUG, and other NCC-specific transcription factors such as MSX1 and TFAP2A (), causing the cells to delaminate and migrate away from the forming neural tube (Figure 1A). The spatial location of NCCs along the anterior-posterior axis of the embryo predefine their paths of migration. The anterior-most cranial NCCs of the forebrain and hindbrain populate the frontonasal process and maxillary arch (Figures 1B,C), contributing to development of the facial skeleton, whereas more posterior cranial NCCs populate the pharyngeal arches to form the musculoskeletal elements of the lower jaw and neck (Figures 1B,C). NCC migration into their target primordia occur in response to cues within the local extracellular environment. Here, as NCCs populate the developing prominences, reciprocal FGF, BMP, SHH, and retinoic acid signalling interactions between mesenchymal NCCs and the epithelial ectoderm and endoderm direct their spatial organization and activate GRNs responsible for proliferation, outgrowth and differentiation of the craniofacial skeleton [(; ; ; ) and references within].
FIGURE 1
2.1 The Origin of Species-Specific Pattern
The specific influence of NCCs patterning the vertebrate head has been showcased through cross-species transplantations and xenografts. These experiments have revealed that NCCs possess intrinsic programming and autonomous behaviours which drive species-specific patterning (). NCC transplantation chimeras in avian embryos see recipient species develop donor-specific patterning, bone formation and craniofacial morphology (; ; ; ). Such morphological outcomes are driven via intrinsic NCC behaviours, including donor-specific regulation of the cell-cycle and distinct expression of transcriptional regulators and signalling factors (). These unique NCC behaviours are further suggested to influence their local environment to produce distinct morphological outcomes. Here, NCC-derived signals modulate activation of reciprocal signalling pathways to the surrounding ectoderm and endoderm which determine gene expression and spatiotemporal patterning of the facial primordia (). In agreement with this, while shared (species-generic) genes and patterning factors are active in the developing facial prominences, each species displays distinct expression profiles during beak outgrowth and development (Wu et al., 2004; Wu et al., 2006; ). Together, these data suggest that intrinsic species-specific NCC programming influences interactions with their local environment, regulating differentiation of craniofacial cells and tissues and the development of distinct morphological identities.
2.2 Marsupial Heterochrony, Accelerated Neural Crest Cell Specification and Migration
The mechanisms underlying mammalian neural crest patterning and craniofacial development have been largely ascertained from studies in mouse. However, while these findings may be relevant for eutherian mammals, comparative studies in marsupials have revealed pronounced heterochrony in their NCC behaviours. During specification at the neural plate border, marsupial NCCs undergo rapid delamination and migration prior to neural plate folding (Figure 1A) (; ; ; ; ), leading to large accumulations of NCCs within the forming facial prominences at an earlier equivalent developmental stage to that seen in eutherians (Figure 1B) (). Remarkably, very little is known about the molecular regulation of marsupial NCCs during development. Two related studies revealed that in the opossum embryo, NCC specification and delamination is accelerated as a result of sequence alteration in a SOX9 enhancer which drives early activation of SOX9 in the neural plate border (; ). This accelerated activation likely influences the heterochronic migration, proliferation, and ossification observed in marsupials, though no other studies have interrogated these processes or drawn comparisons with eutherians. This represents a large gap in our understanding of how NCC behaviours influence development and differ between distinct mammalian clades. Future studies should address the genetic underpinning of these behavioural differences and their contribution to craniofacial patterning. Curiously, it remains to be seen whether transplantation of marsupial NCCs into recipient mouse embryos (or vice versa) would retain their heterochronic behaviours and promote differential establishment of the facial prominences and skeleton. As such, observations into marsupial NCC biology and comparative heterochrony between eutherians are required for a complete understanding of mammalian NCC patterning and craniofacial development.
3 Craniofacial Patterning, Disparity, and Convergence in Therian Mammals
Mammals have evolved unique cranial adaptations which distinguish them from other vertebrates. Evolutionary novelties such as a hinged jaw, middle ear bones and muzzle or semi-motile snout () have allowed mammals to adapt to a diverse range of ecological niches. However, since diverging ∼160 million years ago (), therian mammals (marsupials and eutherians) have evolved distinct reproductive and developmental strategies, resulting in heterochrony and lineage-specific constraints (). The marsupial mode of reproduction requires well-developed jaws and forelimbs at a comparatively early stage to allow the altricial neonate to crawl from the birth canal into pouch and attach to the teat for an extended period of suckling. These distinct functional requirements require differences in the onset of development of the olfactory and central nervous system, and musculoskeletal element of the head body and limbs (; ; ; ; ; ; ). Particularly, during craniofacial development, ossification and suture closure of the facial bones are advanced to meet the functional requirements associated with suckling (; ; ; ). Overall, these constraints imposed on the marsupial orofacial bones are suggested to limit evolvability of their cranial anatomy.
Marsupials have evolved altered patterns of cranial modularity (; ; ; ; ) which are thought to reduce their overall skull shape diversity compared to eutherians (; ). For example, the marsupial jaws form a functionally constrained module, while the frontonasal bones and neurocranium are under relaxed constraint and can evolve more freely (). On the other hand, eutherian mammals largely lack these constraints during development, thus their cranial bone groups are free to evolve independently producing a greater range of morphological adaptations. Importantly, these frontonasal, jaw and neurocranium bone groups (anatomical modules) possess distinct embryonic origins, arising from the cranial NC, first arch NC, or head mesoderm, respectively (developmental modules) (; ; Yoshida et al., 2008). These semi-independent origins, known as mosaicism, allow flexibility in how different cranial morphologies can evolve and change (), even in the presence of functional constraints. Importantly, the combination of cranial mosaicism with cell-autonomous programming of NCCs provide clues as to how particular cranial adaptations can arise during evolution. Specifically, it can be hypothesized that evolution within GRNs associated with cranial progenitor cell types can produce adaptive morphological outcomes.
These evolutionary hypotheses have been recently applied, investigating the origins of the remarkable craniofacial convergence observed between the marsupial thylacine and eutherian wolf (; ). During postnatal ontogeny, the thylacine and wolf frontonasal and neurocranial bones develop with strong shape convergence, whilst the thylacine’s maxillary bones (upper jaw) possess constrained shape shared with other marsupials and disparate patterns to that seen in the wolf (). This supports the notion that adaptive evolution (similarity and disparity) of the mammalian skull is modular (; ), facilitated by mosaic evolution of select bone groups. Furthermore, the distinct embryological origins of the convergent bone groups observed between the thylacine and wolf suggest their underlying GRNs may be convergently targeted by selection. Indeed, comparative genomic investigations of the loci underlying the thylacine and wolf’s cranial convergence revealed enrichment of homoplasy in GRNs associated with cranial mesenchyme migration, differentiation, and ossification (). Taken together, these studies support the hypothesis that evolution within GRNs of embryonic cranial precursors may specify species-specific patterning of the facial primordia, ultimately influencing craniofacial shape. However, this hypothesis requires further validation, particularly into the role of mammalian NCC heterochrony during early facial development and patterning. As such, establishing a marsupial model of NCC patterning and craniofacial biology that is amenable to manipulation is essential to our understanding of how evolutionary adaptations are produced during development.
4 A Marsupial Model to Investigate Mammalian Heterochrony
Modern studies of NCC development and craniofacial patterning in mammals have leveraged the mouse Cre-Lox system, with several transgenic reporter lines established to target various stages of the NCC or skull developmental pathway (Zhang et al., 2002; ; Yoshida et al., 2008; ; ; ). Of these, the Wnt1-cre strain has been widely utilized for NCC developmental biology to uncover the spatiotemporal decisions underlying NCC differentiation (), defining tissue boundaries between NCC and non NCC-derived cranial structures (; ; ), as well as a multipotent NCC line to define models of differentiation (; ). In addition, chromatin profiling of mouse NCCs and craniofacial prominences have annotated the regulatory landscape of craniofacial enhancers and putative GRNs (; ; ; ). Yet while these tools provide powerful and valuable outcomes, they are scarcely utilized outside murine models, limiting comparative mammalian research. Recently however, several new marsupial resources are actively being established, including a pioneering study to generate the first genetically modified marsupials—founder lines of tyrosinase knockout opossums (). Though marsupial transgenic resources are still in their infancy, these advances have primed the generation of new marsupial Cre-Lox resources for developmental investigations. Of note, the generation of a marsupial orthologous WNT1-cre line would allow targeted labelling of neural crest cells and their craniofacial derivatives, opening the door for comparative developmental studies and investigations into mammalian heterochrony.
4.1 The Dunnart as the Gold-Standard Marsupial Model
In the past, several marsupial species have provided insights to various aspects of mammalian biology, reproduction, and development (), with the American opossum (Monodelphis domestica) informing models of NCC and limb development (; ; ; ). However, Monodelphis are basal American marsupials (superorder Ameridelphia) possessing an 80-million-year divergence from Australian marsupials, similar to times shared between human and mouse. Therefore, an Australian laboratory-based marsupial model with similar easy husbandry, year-round breeding and experimental manipulation is still required for a more complete understanding of mammalian (and marsupial) biology. Dunnarts (Sminthopsis sp.; superorder Australidelphia) are small, carnivorous, mouse-like marsupials that are easy to maintain, possess simple husbandry and are polyovular, poly-oestrous and spontaneous ovulators which produce multiple litters of up to 10 pouch young year round (; ; ; ). Owing to this, several new resources are being established for the fat-tailed dunnart (S. crassicaudata, hereafter referred to as the dunnart) as the gold-standard model for next-gen marsupial biology. These include a chromosome level assembly, transcriptomic and gene regulatory datasets, induced pluripotent cells, inbred strains, and transgenic laboratory lines (). Furthermore, like other marsupials, the dunnart possesses significant heterochrony in development of its head, brain and limbs compared with eutherian species, making it an excellent model for comparative mammalian research.
One of the most remarkable features of dunnart biology is its rapid gestation and ultra-altricial state at birth (; ). Dasyurid marsupials, including the dunnart, represent some of the most altricial of all extant mammals. Dunnart neonates are born after a rapid 13.5-day gestation, compared to ∼20 days in mouse (Figure 1D), and superficially resemble a eutherian foetus. At birth, the dunnart orofacial region appears as rudimentary facial prominences akin to an embryonic day 11.5–12 mouse (Figure 1C), despite being functional to accommodate suckling. The newborn dunnart lacks a developed brain and has paddle-like hindlimbs, but possesses highly developed, muscularized forelimbs with claws to accommodate crawling (Figure 1D) (; ). Remarkably, newborn dunnarts lack mineralized bone in the facial skeleton and forelimbs, which rapidly ossify within the first 24 h, while the hindlimbs do not start to ossify until ∼D5 (). This extreme heterochrony and altriciality at birth allows direct manipulations of these developmental systems ex utero, at equivalent eutherian embryonic stages (). Critically, the ultra-altricial birth of dasyurids demand additional acceleration of the onset of NCC specification, migration and proliferation, compared to the opossum (). These features distinguish the dunnart as an exceptional mammalian model to investigate NCC-derived craniofacial patterning and ossification. However, detailed analyses which substantiate these early NCC behaviours in Sminthopsis have yet to be performed, representing an important first step to understand their NCC biology and thus heterochrony in mammals. Nevertheless, the dunnart is well positioned to determine how altered developmental timing influences ontogeny and craniofacial morphogenesis, providing new insights into the origin of species-specific pattern.
5 A Look to the Future: Comparative Evo-Devo-Omics
The age of comparative and functional genomics has accelerated investigations into the molecular basis of mammalian trait evolution. Comparative genomics has allowed identification of genes and regulatory regions under selection within and between lineages (; ; ; , ); comparative bulk RNA-seq has revealed differentially expressed genes between tissues or developing structures (; ); and chromatin pulldown or accessibility assays (ChIP, HiC, or ATAC-seq) define the gene regulatory landscape associated with these tissues or developing structures (; ). However, though powerful, individually these analyses are static and may overlook dynamic processes that contribute to development of complex traits. For example, while identification of differentially expressed genes or enhancers active in the embryonic orofacial region may constitute components that contribute to mammalian facial shape diversity (species-generic), such analyses are unable to capture dynamic regulation of these and the GRNs that influence development of unique anatomical features (species-specific) ()—as exemplified in avian models (; ; ; ). As such, alternative approaches are required to disentangle the complex landscape of craniofacial development between disparate species.
The advent of single-cell omics has revolutionized developmental biology, producing high-resolution atlases of diverse developmental processes (). To date, single-cell studies have been applied to multiple aspects of neural crest patterning and craniofacial development (; ; ; ; ; ), providing unique insights into how these complex developmental processes are regulated. Single-cell transcriptomics (scRNA-seq) allow detailed characterization of transcriptional profiles and cell-types present within developing structures, fate decisions and gene expression dynamics underlying differentiation of progenitors into mature cell types (), and cell-cell signalling interactions between adjacent tissues (). Importantly, scRNA-seq data can be integrated with genome-wide assays for Transposase-Accessible Chromatin (ATAC-seq) to define regulatory elements active within their underlying cell types (; ; ), or spatial transcriptomics to resolve cellular gene expression profiles in individual cells (Xia et al., 2019) or developing tissues in situ (). Used in combination, these techniques provide powerful methods to integrate developmental biology with gene expression dynamics and construction of species-specific GRNs.
Despite their potential, single-cell multi-omic approaches have been scarcely applied in comparative evolutionary biology. Such studies of “comparative evo-devo-omics” between taxa are becoming rapidly viable to investigate the molecular mechanisms underlying convergence, constraint, or innovation in specific developmental processes (; ). However, the lack of these applied studies are largely in response to significant technical limitations surrounding integration and batch correction of disparate datasets, specificity and stage-matching of tissues and homologous cell types between disparate species, and quality of the underlying genome and transcriptome—reviewed by (). Nevertheless, these limitations can be mitigated through application of tools aiding dataset integration, sequencing depth and batch correction, as well as issues with transcriptome quality and gene orthology (; ). Furthermore, new applied methodologies are being produced to better identify and match homologous cell and tissue types (; ; ) and their proportions between distantly related species and datasets (). Given the rapid rate by which these limitations are being resolved by the community, comparative evo-devo-omics presents a powerful platform to interrogate the cell, molecular and developmental mechanisms underlying heterochronic NCC specification and facial patterning between marsupial and eutherian mammals.
5.1 Mammalian Craniofacial Heterochrony at Single Cell Resolution
Using the above examples, I present a hypothetical workflow for detailed investigations into mammalian craniofacial heterochrony and evolution through a comparative lens. First, sampling of single-cell RNA, chromatin and spatial profiles of stage-matched dunnart and mouse embryos (Figure 2A) will allow generation of species-specific transcriptional atlases, building on existing datasets () and producing novel mammalian resources. The resulting transcriptomic, epigenetic and spatial profiles can be clustered and integrated for detection of homologous and novel cell types (; ), conserved and disparate gene co-expression modules (), cell type proportions () and spatial quantification of genes in situ (Figure 2B). From here, evolutionary hypotheses can be tested through identification of dynamic transcriptional, signalling, epigenetic and spatial relationships, revealing shared (species-generic) and unique (species-specific) processes underlying facial development and evolution (Figure 2C). Through application of these approaches, we can begin to determine how NCC gene regulatory architecture differs between therian mammals, and their influence on heterochronic craniofacial patterning. Ultimately, this will not only provide valuable data into how diverse facial shapes are produced during development, but also provide novel insights into how mammalian craniofacial diversity arises during evolution.
FIGURE 2
Statements
Data availability statement
The original contributions presented in the study are included in the article/Supplementary Material, further inquiries can be directed to the corresponding author.
Author contributions
AN conceived the study and wrote the manuscript.
Acknowledgments
I thank my mentors Andrew Pask, Christy Hipsley, Stephen Frankenberg, and Craig Smith for constructive discussions and guidance which led to the preparation of this manuscript.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher’s note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
References
1
AttanasioC.NordA. S.ZhuY.BlowM. J.LiZ.LibertonD. K.et al (2013). Fine Tuning of Craniofacial Morphology by Distant-Acting Enhancers. Science342, 1–20. 10.1126/science.1241006
2
BeirigerA.SearsK. E. (2014). Cellular Basis of Differential Limb Growth in Postnatal Gray Short-Tailed Opossums (Monodelphis Domestica). J. Exp. Zool. Mol. Dev. Evol.)322, 221–229. 10.1002/jez.b.22556
3
BennettC. V.GoswamiA. (2013). Statistical Support for the Hypothesis of Developmental Constraint in Marsupial Skull Evolution. BMC Biol.11. 10.1186/1741-7007-11-52
4
Bininda-EmondsO. R. P.CardilloM.JonesK. E.MacPheeR. D. E.BeckR. M. D.GrenyerR.et al (2007). The Delayed Rise of Present-Day Mammals. Nature446, 507–512. 10.1038/nature05634
5
BrugmannS. A.PowderK. E.YoungN. M.GoodnoughL. H.HahnS. M.JamesA. W.et al (2010). Comparative Gene Expression Analysis of Avian Embryonic Facial Structures Reveals New Candidates for Human Craniofacial Disorders. Hum. Mol. Genet.19, 920–930. 10.1093/hmg/ddp559
6
BuenrostroJ. D.WuB.LitzenburgerU. M.RuffD.GonzalesM. L.SnyderM. P.et al (2015). Single-cell Chromatin Accessibility Reveals Principles of Regulatory Variation. Nature523, 486–490. 10.1038/nature14590
7
ButlerA.HoffmanP.SmibertP.PapalexiE.SatijaR. (2018). Integrating Single-Cell Transcriptomic Data across Different Conditions, Technologies, and Species. Nat. Biotechnol.36, 411–420. 10.1038/nbt.4096
8
CaoJ.CusanovichD. A.RamaniV.AghamirzaieD.PlinerH. A.HillA. J.et al (20182018). Joint Profiling of Chromatin Accessibility and Gene Expression in Thousands of Single Cells. Science361, 1380–1385. 10.1126/science.aau0730
9
CaoJ.SpielmannM.QiuX.HuangX.IbrahimD. M.HillA. J.et al (2019). The Single-Cell Transcriptional Landscape of Mammalian Organogenesis. Nature566, 496–502. 10.1038/s41586-019-0969-x
10
CapraJ. A.ErwinG. D.MckinseyG.RubensteinJ. L. R.PollardK. S. (2013). Many Human Accelerated Regions Are Developmental Enhancers. Phil. Trans. R. Soc. B368, 20130025. 10.1098/rstb.2013.0025
11
ChenC.-C.BalabanE.JarvisE. D. (2012). Interspecies Avian Brain Chimeras Reveal that Large Brain Size Differences Are Influenced by Cell-Interdependent Processes. PLoS One7, e42477. 10.1371/journal.pone.0042477
12
CheungM.BriscoeJ. (2003). Neural Crest Development Is Regulated by the Transcription Factor Sox9. Development130, 5681–5693. 10.1242/dev.00808
13
ChewK. Y.ShawG.YuH.PaskA. J.RenfreeM. B. (2014). Heterochrony in the Regulation of the Developing Marsupial Limb. Dev. Dyn.243, 324–338. 10.1002/dvdy.24062
14
CookL. E.NewtonA. H.HipsleyC. A.PaskA. J. (2021). Postnatal Development in a Marsupial Model, the Fat-Tailed Dunnart Sminthopsis crassicaudata; Dasyuromorphia: Dasyuridae. Commun. Biol.4, 1–14. 10.1038/s42003-021-02506-2
15
CooperK.SaxenaA.SharmaV.NeufeldS.TranM.GutierrezH.et al (2020). Interspecies Transcriptome Analyses Identify Genes that Control the Development and Evolution of Limb Skeletal Proportion. FASEB J.34, 1–1. 10.1096/fasebj.2020.34.s1.00363
16
CoulyG. F.ColteyP. M.Le DouarinN. M. (1993). The Triple Origin of Skull in Higher Vertebrates: a Study in Quail-Chick Chimeras. Development117, 409–429. 10.1242/dev.117.2.409
17
CreuzetS.SchulerB.CoulyG.Le DouarinN. M. (2004). Reciprocal Relationships between Fgf8 and Neural Crest Cells in Facial and Forebrain Development. Proc. Natl. Acad. Sci. U.S.A.101, 4843–4847. 10.1073/pnas.0400869101
18
DashS.TrainorP. A. (2020). The Development, Patterning and Evolution of Neural Crest Cell Differentiation into Cartilage and Bone. Bone137, 115409. 10.1016/j.bone.2020.115409
19
DickelD. E.YpsilantiA. R.PlaR.ZhuY.BarozziI.MannionB. J.et al (2018). Ultraconserved Enhancers Are Required for Normal Development. Cell172, 491–499. e15. 10.1016/j.cell.2017.12.017
20
EalbaE. L.JheonA. H.HallJ.CurantzC.ButcherK. D.SchneiderR. A. (2015). Neural Crest-Mediated Bone Resorption Is a Determinant of Species-specific Jaw Length. Dev. Biol.408, 151–163. 10.1016/j.ydbio.2015.10.001
21
EckalbarW. L.SchlebuschS. A.MasonM. K.GillZ.ParkerA. V.BookerB. M.et al (2016). Transcriptomic and Epigenomic Characterization of the Developing Bat Wing. Nat. Genet.48, 528–536. 10.1038/ng.3537
22
EldridgeM. D. B.DeakinJ. E.MacDonaldA. J.ByrneM.FitzgeraldA.JohnsonR. N.et al (2020). The Oz Mammals Genomics (OMG) Initiative: Developing Genomic Resources for Mammal Conservation at a Continental Scale. Aust. Zool.40, 505–509. 10.7882/AZ.2020.003
23
FabreA.-C.DowlingC.Portela MiguezR.FernandezV.NoiraultE.GoswamiA. (2021). Functional Constraints during Development Limit Jaw Shape Evolution in Marsupials. Proc. R. Soc. B288, 1–8. 10.1098/rspb.2021.0319
24
FarmerD. J. T.MlcochovaH.ZhouY.KoellingN.WangG.AshleyN.et al (2021). The Developing Mouse Coronal Suture at Single-Cell Resolution. Nat. Commun.12, 1–14. 10.1038/s41467-021-24917-9
25
FeiginC. Y.NewtonA. H.DoroninaL.SchmitzJ.HipsleyC. A.MitchellK. J.et al (2018). Genome of the Tasmanian Tiger Provides Insights into the Evolution and Demography of an Extinct Marsupial Carnivore. Nat. Ecol. Evol.2, 182–192. 10.1038/s41559-017-0417-y
26
FeiginC. Y.NewtonA. H.PaskA. J. (2019). Widespread Cis-Regulatory Convergence between the Extinct Tasmanian Tiger and Gray Wolf. Genome Res.29, 1648–1658. 10.1101/gr.244251.118
27
FeliceR. N.GoswamiA. (2018). Developmental Origins of Mosaic Evolution in the Avian Cranium. Proc. Natl. Acad. Sci. U.S.A.115, 555–560. 10.1073/pnas.1716437115
28
FeregrinoC.TschoppP. (2021). Assessing Evolutionary and Developmental Transcriptome Dynamics in Homologous Cell Types. Dev. Dyn., 1–18. 10.1002/dvdy.384
29
FishJ. L. (2019). Evolvability of the Vertebrate Craniofacial Skeleton. Seminars Cell & Dev. Biol.91, 13–22. 10.1016/j.semcdb.2017.12.004
30
FooteA. D.LiuY.ThomasG. W. C.VinařT.AlföldiJ.DengJ.et al (2015). Convergent Evolution of the Genomes of Marine Mammals. Nat. Genet.47, 272–275. 10.1038/ng.3198
31
FrigoL.WoolleyP. A. (1997). Growth and Development of Pouch Young of the Stripe-Faced Dunnart, Sminthopsis Macroura (Marsupialia : Dasyuridae), in Captivity. Aust. J. Zool.45, 157–170. 10.1071/ZO97002
32
FrigoL.WoolleyP. (1996). Development of the Skeleton of the Stripe-Faced Dunnart, Sminthopsis Macroura (Marsupialia: Dasyuridae). Aust. J. Zool.44, 155–164. 10.1071/ZO9960155
33
GoswamiA. (2007). Cranial Modularity and Sequence Heterochrony in Mammals. Evol. Dev.9, 290–298. 10.1111/j.1525-142X.2007.00161.x
34
GoswamiA. (2006). Cranial Modularity Shifts during Mammalian Evolution. Am. Nat.168, 270–280. 10.1086/505758
35
GoswamiA.MilneN.WroeS. (2011). Biting through Constraints: Cranial Morphology, Disparity and Convergence across Living and Fossil Carnivorous Mammals. Proc. R. Soc. B278, 1831–1839. 10.1098/rspb.2010.2031
36
GoswamiA.PollyP. D.MockO. B.Sánchez-villagraM. R. (2012). Shape, Variance and Integration during Craniogenesis: Contrasting Marsupial and Placental Mammals. J. Evol. Biol.25, 862–872. 10.1111/j.1420-9101.2012.02477.x
37
GoswamiA.PollyP. D. (2010). The Influence of Modularity on Cranial Morphological Disparity in Carnivora and Primates (Mammalia). PLoS One5, e9517–8. 10.1371/journal.pone.0009517
38
GoswamiA.RandauM.PollyP. D.WeisbeckerV.BennettC. V.HautierL.et al (2016). Do developmental Constraints and High Integration Limit the Evolution of the Marsupial Oral Apparatus?Integr. Comp. Biol.56, 404–415. 10.1093/icb/icw039
39
GoswamiA.WeisbeckerV.Sánchez-VillagraM. R. (2009). Developmental Modularity and the Marsupial-Placental Dichotomy. J. Exp. Zool.312B, 186–195. 10.1002/jez.b.21283
40
GreenS. A.Simoes-costaM.BronnerM. E. (2015). Evolution of Vertebrates as Viewed from the Crest. Nature520, 474–482. 10.1038/nature14436
41
HaghverdiL.LunA. T. L.MorganM. D.MarioniJ. C. (2018). Batch Effects in Single-Cell RNA-Sequencing Data Are Corrected by Matching Mutual Nearest Neighbors. Nat. Biotechnol.36, 421–427. 10.1038/nbt.4091
42
HallJ.JheonA. H.EalbaE. L.EamesB. F.ButcherK. D.MakS.-S.et al (2014). Evolution of a Developmental Mechanism: Species-specific Regulation of the Cell Cycle and the Timing of Events during Craniofacial Osteogenesis. Dev. Biol.385, 380–395. 10.1016/j.ydbio.2013.11.011
43
HigashiyamaH.KoyabuD.HirasawaT.WerneburgI.KurataniS.KuriharaH. (2021). Mammalian Face as an Evolutionary Novelty. Proc. Natl. Acad. Sci. U.S.A.118, 1–8. 10.1073/pnas.2111876118
44
HuQ.UenoN.BehringerR. R. (2004). Restriction of BMP4 Activity Domains in the Developing Neural Tube of the Mouse Embryo. EMBO Rep.5, 734–739. 10.1038/sj.embor.7400184
45
IshiiM.AriasA. C.LiuL.ChenY.-B.BronnerM. E.MaxsonR. E. (2012). A Stable Cranial Neural Crest Cell Line from Mouse. Stem Cells Dev.21, 3069–3080. 10.1089/scd.2012.0155
46
JiangX.IsekiS.MaxsonR. E.SucovH. M.Morriss-KayG. M. (2002). Tissue Origins and Interactions in the Mammalian Skull Vault. Dev. Biol.241, 106–116. 10.1006/dbio.2001.0487
47
JinS.Guerrero-JuarezC. F.ZhangL.ChangI.RamosR.KuanC.-H.et al (2021). Inference and Analysis of Cell-Cell Communication Using CellChat. Nat. Commun.12, 1–20. 10.1038/s41467-021-21246-9
48
KeyteA. L.SmithK. K. (2010). Developmental Origins of Precocial Forelimbs in Marsupial Neonates. Development137, 4283–4294. 10.1242/dev.049445
49
KeyteA.SmithK. K. (2012). Heterochrony in Somitogenesis Rate in a Model Marsupial,Monodelphis Domestica. Evol. Dev.14, 93–103. 10.1111/j.1525-142X.2011.00524.x
50
KiyonariH.KanekoM.AbeT.ShiraishiA.YoshimiR.InoueK.-i.et al (2021). Targeted Gene Disruption in a Marsupial, Monodelphis Domestica, by CRISPR/Cas9 Genome Editing. Curr. Biol.31, 3956–3963. 10.1016/j.cub.2021.06.056
51
KurataniS.KusakabeR.HirasawaT. (2018). The Neural Crest and Evolution of the Head/trunk Interface in Vertebrates. Dev. Biol.444, S60–S66. 10.1016/j.ydbio.2018.01.017
52
LewisA. E.VasudevanH. N.O’NeillA. K.SorianoP.BushJ. O. (2013). The Widely Used Wnt1-Cre Transgene Causes Developmental Phenotypes by Ectopic Activation of Wnt Signaling. Dev. Biol.379, 229–234. 10.1016/j.ydbio.2013.04.026
53
LiH.JonesK. L.HooperJ. E.WilliamsT. (2019). The Molecular Anatomy of Mammalian Upper Lip and Primary Palate Fusion at Single Cell Resolution. Dev146, dev174888. 10.1242/dev.174888
54
MahadevaiahS. K.SangrithiM. N.HirotaT.TurnerJ. M. A. (2020). A Single-Cell Transcriptome Atlas of Marsupial Embryogenesis and X Inactivation. Nature586, 612–617. 10.1038/s41586-020-2629-6
55
MartikM. L.BronnerM. E. (2021). Riding the Crest to Get a Head: Neural Crest Evolution in Vertebrates. Nat. Rev. Neurosci.22, 616–626. 10.1038/s41583-021-00503-2
56
MartinK. E. A.MackayS. (2003). Postnatal Development of the Fore- and Hindlimbs in the Grey Short-Tailed Opossum, Monodelphis Domestica. J. Anat.202, 143–152. 10.1046/j.1469-7580.2003.00149.x
57
MarxV. (2021). Method of the Year: Spatially Resolved Transcriptomics. Nat. Methods18, 9–14. 10.1038/s41592-020-01033-y
58
MinouxM.RijliF. M. (2010). Molecular Mechanisms of Cranial Neural Crest Cell Migration and Patterning in Craniofacial Development. Development137, 2605–2621. 10.1242/dev.040048
59
MorrisonJ. A.McLennanR.TeddyJ. M.ScottA. R.Kasemeier-KulesaJ. C.GogolM. M.et al (2021). Single-cell Reconstruction with Spatial Context of Migrating Neural Crest Cells and Their Microenvironments during Vertebrate Head and Neck Formation. Dev148, dev199468. 10.1242/dev.199468
60
Murillo-RincónA. P.KauckaM. (2020). Insights Into the Complexity of Craniofacial Development From a Cellular Perspective. Front. Cell Dev. Biol.8, 1–8. 10.3389/fcell.2020.620735
61
NewtonA. H.FeiginC. Y.PaskA. J. (2017). RUNX2 Repeat Variation Does Not Drive Craniofacial Diversity in Marsupials. BMC Evol. Biol.17, 1–9. 10.1186/s12862-017-0955-6–
62
NewtonA. H.PaskA. J. (2020). Evolution and Expansion of the RUNX2 QA Repeat Corresponds with the Emergence of Vertebrate Complexity. Commun. Biol.3, 771. 10.1038/s42003-020-01501-3
63
NewtonA. H.WeisbeckerV.PaskA. J.HipsleyC. A. (2021). Ontogenetic Origins of Cranial Convergence between the Extinct Marsupial Thylacine and Placental Gray Wolf. Commun. Biol.4, 51. 10.1038/s42003-020-01569-x
64
NguyenB. H.IshiiM.MaxsonR. E.WangJ. (2018). Culturing and Manipulation of O9-1 Neural Crest Cells. J. Vis. Exp.9, 58346. 10.3791/58346
65
NunnC. L.SmithK. K. (1998). Statistical Analyses of Developmental Sequences: The Craniofacial Region in Marsupial and Placental Mammals. Am. Nat.152, 82–101. 10.1086/286151
66
PagellaP.de Vargas RoditiL.StadlingerB.MoorA. E.MitsiadisT. A. (2021). A Single-Cell Atlas of Human Teeth. iScience24, 102405. 10.1016/j.isci.2021.102405
67
PaolinoA.FenlonL. R.KozulinP.RichardsL. J.SuárezR. (2018). Multiple Events of Gene Manipulation via in Pouch Electroporation in a Marsupial Model of Mammalian Forebrain Development. J. Neurosci. Methods293, 45–52. 10.1016/j.jneumeth.2017.09.004
68
ParkerJ.TsagkogeorgaG.CottonJ. A.LiuY.ProveroP.StupkaE.et al (2013). Genome-wide Signatures of Convergent Evolution in Echolocating Mammals. Nature502, 228–231. 10.1038/nature12511
69
PhipsonB.SimC. B.PorrelloE.HewittA. W.PowellJ.OshlackA. (2021). Propeller: Testing for Differences in Cell Type Proportions in Single Cell Data. bioRxiv2021, 470236. 10.1101/2021.11.28.470236
70
RagerL.HautierL.ForasiepiA.GoswamiA.Sánchez-VillagraM. R. (2014). Timing of Cranial Suture Closure in Placental Mammals: Phylogenetic Patterns, Intraspecific Variation, and Comparison with Marsupials. J. Morphol.275, 125–140. 10.1002/jmor.20203
71
RauchA.SeitzS.BaschantU.SchillingA. F.IllingA.StrideB.et al (2010). Glucocorticoids Suppress Bone Formation by Attenuating Osteoblast Differentiation via the Monomeric Glucocorticoid Receptor. Cell Metab.11, 517–531. 10.1016/j.cmet.2010.05.005
72
RoddaS. J.McMahonA. P. (2006). Distinct Roles for Hedgehog and Canonical Wnt Signaling in Specification,differentiation and Maintenance of Osteoblast Progenitors. Development133, 3231–3244. 10.1242/dev.02480
73
SamuelsB. D.AhoR.BrinkleyJ. F.BugacovA.FeingoldE.FisherS.et al (2020). FaceBase 3: Analytical Tools and FAIR Resources for Craniofacial and Dental Research. Development (Cambridge, England), 147(18), dev191213. 10.1242/dev.191213
74
Sánchez-VillagraM. R.GoswamiA.WeisbeckerV.MockO.KurataniS. (2008). Conserved Relative Timing of Cranial Ossification Patterns in Early Mammalian Evolution. Evol. Dev.10, 519–530. 10.1111/j.1525-142X.2008.00267.x
75
SchneiderR. A.HelmsJ. A. (2003). The Cellular and Molecular Origins of Beak Morphology. Science299, 565–568. 10.1126/science.1077827
76
SchneiderR. A. (2018). Neural Crest and the Origin of Species-specific Pattern. Genesis56, e23219–33. 10.1002/dvg.23219
77
SearsK. E. (2009). Differences in the Timing of Prechondrogenic Limb Development in Mammals: The Marsupial-Placental Dichotomy Resolved. Evol. (N. Y).63, 2193–2200. 10.1111/j.1558-5646.2009.00690.x
78
SelwoodL.CoulsonG. (2006). Marsupials as Models for Research. Aust. J. Zool.54, 137. 10.1071/ZOv54n3_IN
79
ShaferM. E. R. (2019). Cross-Species Analysis of Single-Cell Transcriptomic Data. Front. Cell Dev. Biol.7, 1–9. 10.3389/fcell.2019.00175
80
SmithK. K. (1997). Comparative Patterns of Craniofacial Development in Eutherian and Metatherian Mammals. Evolution51, 1663. 10.2307/2411218
81
SmithK. K. (2001). Early Development of the Neural Plate, Neural Crest and Facial Region of Marsupials. J. Anat.199, 121–131. 10.1017/S002187820100820210.1046/j.1469-7580.2001.19910121.x
82
SmithK. K. (2020). J P Hill and Katherine Watson's Studies of the Neural Crest in Marsupials. J. Morphol.281, 1567–1587. 10.1002/jmor.21270
83
SoldatovR.KauckaM.KastritiM. E.PetersenJ.ChontorotzeaT.EnglmaierL.et al (2019). Spatiotemporal Structure of Cell Fate Decisions in Murine Neural Crest. Science364, eaas9536. 10.1126/science.aas9536
84
SpiekmanS. N. F.WerneburgI. (2017). Patterns in the Bony Skull Development of Marsupials: High Variation in Onset of Ossification and Conserved Regions of Bone Contact. Sci. Rep.7, 1–11. 10.1038/srep43197
85
StineZ. E.HuynhJ. L.LoftusS. K.GorkinD. U.SalmasiA. H.NovakT.et al (2009). Oligodendroglial and Pan-Neural Crest Expression of Cre Recombinase Directed bySox10enhancer. Genesis47, 765–770. 10.1002/dvg.20559
86
StuartT.ButlerA.HoffmanP.HafemeisterC.PapalexiE.MauckW. M.et al (2019). Comprehensive Integration of Single-Cell Data. Cell177, 1888–1902. e21. 10.1016/j.cell.2019.05.031
87
SuárezR.PaolinoA.KozulinP.FenlonL. R.MorcomL. R.EnglebrightR.et al (2017). Development of Body, Head and Brain Features in the Australian Fat-Tailed Dunnart (Sminthopsis crassicaudata; Marsupialia: Dasyuridae); A Postnatal Model of Forebrain Formation. PLoS One12, e0184450–18. 10.1371/journal.pone.0184450
88
Szabo-rogersH. L.SmithersL. E.YakobW.LiuK. J. (2010). New Directions in Craniofacial Morphogenesis. Dev. Biol.341, 84–94. 10.1016/j.ydbio.2009.11.021
89
TatarakisD.CangZ.WuX.SharmaP. P.KarikomiM.MacLeanA. L.et al (2021). Single-cell Transcriptomic Analysis of Zebrafish Cranial Neural Crest Reveals Spatiotemporal Regulation of Lineage Decisions during Development. Cell Rep.37, 110140. 10.1016/j.celrep.2021.110140
90
ToschesM. A.YamawakiT. M.NaumannR. K.JacobiA. A.TushevG.LaurentG. (2018). Evolution of Pallium, hippocampus, and Cortical Cell Types Revealed by Single-Cell Transcriptomics in Reptiles. Science.360, 881–888. 10.1126/science.aar4237
91
TrapnellC.CacchiarelliD.GrimsbyJ.PokharelP.LiS.MorseM.et al (2014). The Dynamics and Regulators of Cell Fate Decisions Are Revealed by Pseudotemporal Ordering of Single Cells. Nat. Biotechnol.32, 381–386. 10.1038/nbt.2859
92
UsuiK.TokitaM. (2018). Creating Diversity in Mammalian Facial Morphology: A Review of Potential Developmental Mechanisms. Evodevo9, 1–17. 10.1186/s13227-018-0103-4
93
VagliaJ. L.SmithK. K. (2003). Early Differentiation and Migration of Cranial Neural Crest in the Opossum, Monodelphis Domestica. Evol. Dev.5, 121–135. 10.1046/j.1525-142X.2003.03019.x
94
ViselA.BlowM. J.LiZ.ZhangT.AkiyamaJ. A.HoltA.et al (2009a). ChIP-seq Accurately Predicts Tissue-specific Activity of Enhancers. Nature457, 854–858. 10.1038/nature07730
95
ViselA.RubinE. M.PennacchioL. A. (2009b). Genomic Views of Distant-Acting Enhancers. Nature461, 199–205. 10.1038/nature08451
96
WakamatsuY.NomuraT.OsumiN.SuzukiK. (2014). Comparative Gene Expression Analyses Reveal Heterochrony forSox9expression in the Cranial Neural Crest during Marsupial Development. Evol. Dev.16, 197–206. 10.1111/ede.12083
97
WakamatsuY.SuzukiK. (2019). Sequence Alteration in the Enhancer Contributes to the Heterochronic Sox9 Expression in Marsupial Cranial Neural Crest. Dev. Biol.456, 31–39. 10.1016/j.ydbio.2019.08.010
98
WeisbeckerV.GoswamiA.WroeS.Sánchez-VillagraM. R. (2008). Ossification Heterochrony in the Therian Postcranial Skeleton and the Marsupial-Placental Dichotomy. Evol. (N. Y).62, 2027–2041. 10.1111/j.1558-5646.2008.00424.x
99
WelchJ. D.KozarevaV.FerreiraA.VanderburgC.MartinC.MacoskoE. Z. (2019). Single-Cell Multi-Omic Integration Compares and Contrasts Features of Brain Cell Identity. Cell177, 1873–1887. e17. 10.1016/j.cell.2019.05.006
100
WilkieA. O. M.Morriss-KayG. M. (2001). Genetics of Craniofacial Development and Malformation. Nat. Rev. Genet.2, 458–468. 10.1038/35076601
101
WuP.JiangT.-X.ShenJ.-Y.WidelitzR. B.ChuongC.-M. (2006). Morphoregulation of Avian Beaks: Comparative Mapping of Growth Zone Activities and Morphological Evolution. Dev. Dyn.235, 1400–1412. 10.1002/dvdy.20825
102
WuP.JiangT.-X.SuksaweangS.WidelitzR. B.ChuongC.-M. (2004). Molecular Shaping of the Beak. Science305, 1465–1466. 10.1126/science.1098109
103
XiaC.FanJ.EmanuelG.HaoJ.ZhuangX. (2019). Spatial Transcriptome Profiling by MERFISH Reveals Subcellular RNA Compartmentalization and Cell Cycle-dependent Gene Expression. Proc. Natl. Acad. Sci. U.S.A.116, 19490–19499. 10.1073/pnas.1912459116
104
YoshidaT.VivatbutsiriP.Morriss-KayG.SagaY.IsekiS. (2008). Cell Lineage in Mammalian Craniofacial Mesenchyme. Mech. Dev.125, 797–808. 10.1016/j.mod.2008.06.007
105
ZhangM.XuanS.BouxseinM. L.Von StechowD.AkenoN.FaugereM. C.et al (2002). Osteoblast-specific Knockout of the Insulin-like Growth Factor (IGF) Receptor Gene Reveals an Essential Role of IGF Signaling in Bone Matrix Mineralization. J. Biol. Chem.277, 44005–44012. 10.1074/jbc.M208265200
Summary
Keywords
NCC, mammal, heterochrony, constraint, evolution, GRN, skull
Citation
Newton AH (2022) Marsupials and Multi-Omics: Establishing New Comparative Models of Neural Crest Patterning and Craniofacial Development. Front. Cell Dev. Biol. 10:941168. doi: 10.3389/fcell.2022.941168
Received
11 May 2022
Accepted
06 June 2022
Published
23 June 2022
Volume
10 - 2022
Edited by
Neva P. Meyer, Clark University, United States
Reviewed by
Shunsuke Suzuki, Shinshu University, Japan
Anna Keyte, The Rockefeller University, United States
Updates
Copyright
© 2022 Newton.
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: Axel H. Newton, axel.newton@unimelb.edu.au
† ORCID: Axel H. Newton, orcid.org/0000-0001-7175-5978
This article was submitted to Evolutionary Developmental Biology, a section of the journal Frontiers in Cell and Developmental Biology
Disclaimer
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.