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Ontogenetic Origins of Cranial Convergence Between the Extinct Marsupial Thylacine and Placental Gray Wolf ✉ ✉ Axel H

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Ontogenetic Origins of Cranial Convergence Between the Extinct Marsupial Thylacine and Placental Gray Wolf ✉ ✉ Axel H ARTICLE https://doi.org/10.1038/s42003-020-01569-x OPEN Ontogenetic origins of cranial convergence between the extinct marsupial thylacine and placental gray wolf ✉ ✉ Axel H. Newton 1,2,3 , Vera Weisbecker 4, Andrew J. Pask2,3,5 & Christy A. Hipsley 2,3,5 1234567890():,; Phenotypic convergence, describing the independent evolution of similar characteristics, offers unique insights into how natural selection influences developmental and molecular processes to generate shared adaptations. The extinct marsupial thylacine and placental gray wolf represent one of the most extraordinary cases of convergent evolution in mammals, sharing striking cranial similarities despite 160 million years of independent evolution. We digitally reconstructed their cranial ontogeny from birth to adulthood to examine how and when convergence arises through patterns of allometry, mosaicism, modularity, and inte- gration. We find the thylacine and wolf crania develop along nearly parallel growth trajec- tories, despite lineage-specific constraints and heterochrony in timing of ossification. These constraints were found to enforce distinct cranial modularity and integration patterns during development, which were unable to explain their adult convergence. Instead, we identify a developmental origin for their convergent cranial morphologies through patterns of mosaic evolution, occurring within bone groups sharing conserved embryonic tissue origins. Inter- estingly, these patterns are accompanied by homoplasy in gene regulatory networks asso- ciated with neural crest cells, critical for skull patterning. Together, our findings establish empirical links between adaptive phenotypic and genotypic convergence and provides a digital resource for further investigations into the developmental basis of mammalian evolution. 1 School of Biomedical Sciences, Monash University, Melbourne, VIC, Australia. 2 School of BioSciences, The University of Melbourne, Melbourne, VIC, Australia. 3 Department of Sciences, Museums Victoria, Melbourne, VIC, Australia. 4 College of Science and Engineering, Flinders University, Adelaide, SA, ✉ Australia. 5These authors contributed equally: Andrew J. Pask, Christy A. Hipsley. email: [email protected]; [email protected] COMMUNICATIONS BIOLOGY | (2021) 4:51 | https://doi.org/10.1038/s42003-020-01569-x | www.nature.com/commsbio 1 ARTICLE COMMUNICATIONS BIOLOGY | https://doi.org/10.1038/s42003-020-01569-x hen the first European settlers arrived on the remote bones16,43, which has been suggested to limit marsupial cranial Australian island state of Tasmania, they were aston- disparity38 and integration of the developing oral region41.How- W fi ished to nd a large, striped dog-like animal which, ever, the existence of marsupial “developmental constraint” has unlike other canids, had an abdominal pouch where it reared its been challenged because marsupials have not always possessed young. Appropriately named Thylacinus cynocephalus, translating limited diversity compared with placental mammals44, and do not to “pouched-dog dog-headed”1,2, the marsupial thylacine displayed appear to exhibit adaptive constraints on forelimb45,46 or skull remarkable similarities to placental canids3–5,despitelastsharinga shape variation47. Nevertheless, despite these differences, the common ancestor over 160 million years ago6.Thethylacineand remarkable convergence of cranial shape between adult thylacines gray wolf (Canis lupus) are considered one of the most striking and wolves suggest the independent evolution of similar underlying cases of convergent evolution in mammals, independently evolving developmental processes. nearly identical skull shapes7 in response to shared carnivorous and Recent comparisons between the thylacine and wolf genomes7 predatory ecologies8–11, despite differences in their post-cranial revealed extensive homoplasy in regulatory regions controlling anatomy11,12. This example of convergent evolution offers an craniofacial development48, suggesting the evolution of shared opportunity to determine how natural selection influences devel- molecular pathways underlying their convergence. In this study, we opmental and molecular processes to generate similar further examine the developmental processes that have led to the characteristics13,14. Comparative studies of mammalian ontogeny extraordinary cranial convergence between the extinct thylacine and have provided important insights into differences underlying mar- gray wolf3,7, building on a rare developmental series of thylacine supial and placental development15–18 and how developmental pouch young49. By applying X-ray computed tomography (CT) to mode can impact early cranial ontogeny19. Building on these preserved museum specimens, we describe the cranial ontogeny of comparisons, we can explicitly test whether distantly related species the thylacine and wolf from birth to adulthood, drawing compar- with convergent morphologies have evolved homoplasy in devel- isons with five extant marsupial species. Using 3D landmark and opmental and molecular pathways to establish similarities in skull point cloud-based geometric morphometric analyses, we examine shape. the onset and extent of cranial similarity in ontogenetic and allo- Development of the vertebrate skull is a deeply conserved process metric growth patterns to determine how these are correlated achieved through defined genetic cascades and cellular behaviors throughout development. We specifically examine whether there is during early embryogenesis20. The cranial bones arise from three greater similarity between cranial regions with conserved embryonic distinct embryological origins: the frontonasal process (FNP), first tissue origins, linking phenotypic convergence with genetic homo- pharyngeal arch (PA), and paraxial mesoderm (MES). The FNP plasy in craniofacial tissues48. In addition, we examine module and PA are generated from independent streams of ectoderm- covariation patterns between the thylacine and wolf throughout key derived neural crest cells (NC) and form the bones of the anterior stages of development, to determine whether their adaptive cranial facial skeleton, whereas cells from the paraxial head mesoderm shapes arise through homoplasious modularity and integration (MES) form the bones of the posterior neurocranium20–22.Each patterns. Our findings offer novel insights into the mechanisms stream of cranial mesenchymal cells possesses their own intrinsic underlying mammalian evolution and provide new information on genetic programming, which directs specific patterns of cellular the cranial ontogeny of an extinct species. migration, proliferation, and ossification to form individual bone groups20,23,24. These cranial precursors form discrete develop- mental modules, where each cranial region can evolve and respond Results to selection independently, known as mosaicism (or modularity)25. Ontogenetic allometry. We sampled crania covering the complete However, modularity patterns can also shift throughout ontogeny26. developmental trajectories for the wolf, thylacine, and five addi- During growth and maturation, bones arising from discrete devel- tional extant marsupials, where specimens were available. These opmental modules can group into larger, integrated (co-varied) included the brush-tail possum (Trichosurus vulpecula), koala traits27 in response to changing selective pressures28.Assuch, (Phascolarctos cinereus), woylie (Bettongia penicillata), Eastern quoll modularity and integration are important drivers of phenotypic (Dasyurus viverrinus), and dunnart (Sminthopsis sp.). Crania were evolution, where modules with shared developmental or functional sampled to cover growth from earliest neonatal stages with nearly associations can be uniquely shaped by selection25,29–31.Evolu- completely closed cranial sutures, to full-grown adults. The thyla- tionary shifts in modularity have been shown to facilitate or con- cine and wolf exhibit lineage-specific developmental patterns, strain morphological variation28,31,32, or when selection favors exhibiting distinct heterochrony in their cranial ontogeny. Wolves similar trait integration patterns among species, can promote the are born after a gestation of ~ 65 days in a relatively altricial state evolution of convergent phenotypes3,26,33,34. but possess a largely ossified skull50,51 (mean skull length 54.3 mm; The homologous organization and modular hierarchy of the n = 4, Supplementary data 1), with closure of all major cranial mammalian skull provides an ideal system for examining the sutures except between the parietal and occipital, which remains influence of functional, developmental, and genetic associations partially open. At birth the wolf is substantially larger and more underlying convergent phenotypes. Therian (marsupial and pla- developed than the hyper-altricial thylacine, which by 1.5 weeks cental) mammals display a remarkably conserved pattern of six after its ~21–35 day gestation52 had a total skull length of 12 mm cranial modules, recovered from both fossil and extant species35. (n = 1, Supplementary data 1) and retained open sutures between However, integration, or between-module covariation patterns, all major cranial bones49. By ~1.25-months-old, the thylacine differ between marsupials and placentals, likely in response to their showed equivalence in skull length (~31 mm) and development to a dichotomous modes of reproduction36,37. Placental mammals fetal wolf (36 mm; Fig. 1A) but did not appear morphologically typically develop through an extended
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