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Anomalously High Variation in Postnatal Development Is Ancestral for Dinosaurs but Lost in Birds

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Anomalously High Variation in Postnatal Development Is Ancestral for Dinosaurs but Lost in Birds Anomalously high variation in postnatal development is ancestral for dinosaurs but lost in birds Christopher T. Griffina,1 and Sterling J. Nesbitta aDepartment of Geosciences, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061 Edited by Neil H. Shubin, The University of Chicago, Chicago, IL, and approved November 3, 2016 (received for review August 19, 2016) Compared with all other living reptiles, birds grow extremely fast sequence analysis (OSA) (32) to reconstruct growth sequences of and possess unusually low levels of intraspecific variation during these early dinosaurs, two avian species (Branta canadensis and postnatal development. It is now clear that birds inherited their high Meleagris gallopavo), and a single crocodylian species (Alligator rates of growth from their dinosaurian ancestors, but the origin of mississippiensis), and demonstrate that the earliest dinosaurs the avian condition of low variation during development is poorly developed differently than living archosaurs. constrained. The most well-understood growth trajectories of later Mesozoic theropods (e.g., Tyrannosaurus, Allosaurus)showsimilarly Results low variation to birds, contrasting with higher variation in extant Our OSAs indicate that both C. bauri and M. rhodesiensis pos- crocodylians. Here, we show that deep within Dinosauria, among sessed a high level of intraspecific variation, both in sequence the earliest-diverging dinosaurs, anomalously high intraspecific var- polymorphism and in body size at different levels of morpho- iation is widespread but then is lost in more derived theropods. This logical maturity (Figs. 1 and 2). Analysis of the 27 ontogenetic style of development is ancestral for dinosaurs and their closest characters for C. bauri reconstructed 136 equally parsimonious relatives, and, surprisingly, this level of variation is far higher than developmental sequences (Fig. 1 and SI Appendix,Fig.S4), with in living crocodylians. Among early dinosaurs, this variation is wide- the modal sequence representing only 12.57% the support weight of spread across Pangaea in the Triassic and Early Jurassic, and among all semaphoronts [unique suites of developmental characters, early-diverging theropods (ceratosaurs), this variation is maintained modified from (33)]. Because of missing data, many sequences were for 165 million years to the end of the Cretaceous. Because the Late highly unresolved, and so this number of sequences is a lower bound Triassic environment across Pangaea was volatile and heteroge- for the amount of variation in the sample during life. OSA for the neous, this variation may have contributed to the rise of dinosau- 10 femoral ontogenetic characters of C. bauri resulted in 82 de- rian dominance through the end of the Triassic Period. velopmental sequences (Fig. 2A and SI Appendix,Fig.S7), and for M. rhodesiensis, 145 developmental sequences (Fig. 2B and SI Appendix,Fig.S8) were reconstructed for 13 femoral characters. ontogeny | variation | dinosaur | Triassic | extinction In contrast, the extant birds possess low levels of intraspecific variation relative to early theropods, consistent with other n comparison with other reptiles, avian biology is highly un- studies (10, 11). The OSA of 36 ontogenetic characters of EVOLUTION Iusual, characterized by “hollow” bones and postcranial skeletal B. canadensis returned 9 equally parsimonious developmental pneumaticity, feathers, a unique forelimb digit formula, endo- sequences (Fig. 3A and SI Appendix, Fig. S9), with a modal thermy, and rapid growth rates. However, these peculiarities sequence possessing 87.22% of the support weight of all sem- initially arose in nonavian dinosaurs (1–7) in a gradual process aphoronts combined. The femoral characters in this dataset were occurring over tens of millions of years (8, 9). In addition to their poorly resolved, but OSA of the dataset of Tumarkin-Deratzian extremely rapid rates of growth, avian ontogeny possesses a et al. (11) of 18 femoral characters of B. canadensis showed similarly characteristically low level of morphological variation within a low variation, returning 12 sequences (Fig. 3B and SI Appendix,Fig. species relative to that of other reptiles. The majority of indi- S10) and a modal sequence consisting of 92% of all combined viduals in a given avian species undergoes the same morpho- EARTH, ATMOSPHERIC, logical changes during ontogeny in the same order at similar Significance AND PLANETARY SCIENCES body sizes (10, 11), whereas their closest living relatives, croco- – dylians, possess higher variation (10, 12 14). How and when this Birds—the fastest growing terrestrial vertebrates—develop feature of avian biology evolved is poorly constrained. unlike all other living reptiles. As part of this postnatal de- This avian style of development must have evolved after its velopmental mode, birds possess a low amount of intraspecific most recent common ancestor with crocodylians but before the variation, and the timing of the origin of this low variation is origin of Aves. Most studies of the ontogeny of more-derived poorly constrained. By studying well-sampled growth series of theropods (15–17) suggest that the low levels of variation that nonavian dinosaurs and their closest relatives, we were able to characterize avian ontogeny were present in close nonavian relatives identify this transition within Mesozoic theropod dinosaurs. as well. Closer to the origin of Dinosauria, morphological variation within species is widespread (18–26), but whether this variation is Surprisingly, the earliest dinosaurs and their close relatives the result of taxonomic diversity, ontogeny, sexual dimorphism, or possessed an extremely high amount of variation, higher than simple individual variation is not clear (22, 23, 27). Furthermore, either crocodylians or birds. This high variation is the ancestral close dinosaurian relatives or “dinosaur precursors” (e.g., Silesaurus, dinosaurian scheme and was lost in more derived nonavian Asilisaurus) possess high intraspecific variation in growth sequences theropods, including Allosaurus and Tyrannosaurus. High var- [i.e., sequence polymorphism (28)], suggesting that this condition iation could have contributed to the rise of dinosaurian domi- could be ancestral for Dinosauria (21). nance during the Triassic–Jurassic mass extinction. In contrast to most of the early dinosaurian record, which rarely preserves greater than a single individual per species (29, 30), Author contributions: C.T.G. and S.J.N. designed research; C.T.G. performed research; C.T.G. the theropod Coelophysis bauri is known from the most well- analyzed data; and C.T.G. and S.J.N. wrote the paper. sampled growth series of any nonavian dinosaur preserved as a The authors declare no conflict of interest. single population in the same horizon (31). We used this taxon as This article is a PNAS Direct Submission. a lens to interpret development among early dinosaurs, with ad- 1To whom correspondence should be addressed. Email: [email protected]. ditional support from another early dinosaur with a well-sampled This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. growth series, Megapnosaurus rhodesiensis (24). We used ontogenetic 1073/pnas.1613813113/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1613813113 PNAS | December 20, 2016 | vol. 113 | no. 51 | 14757–14762 Downloaded by guest on September 27, 2021 28 hypothesized mature states of these characters are not attained Modal sequence 27 in a single ontogenetic step but are staggered in appearance in Character state developmental sequences, along which individuals progress to- 26 transition Unobserved, ward morphological maturity in a stepwise fashion. Instead of a 25 reconstructed semaphoront single path of semaphoronts leading from the least to most 24 Semaphoront mature, semaphoronts of both M. rhodesiensis and C. bauri are 23 Representative Femoral arranged along many developmental sequences (Figs. 1 and 2). Length (mm) 22 Additionally, although size is often used as a proxy for degree of – 21 109.7 mm 220.6 mmm skeletal maturity in many studies (20, 24, 34 41), size correlates 20 poorly with morphological maturity, as quantified by maturity score in OSA, even though OSA may reconstruct missing data as 19 present and thus raise the maturity score higher than a strict 18 scoring of the individual would give (Figs. 1 and 2). Therefore, 17 skeletally mature individuals could possess a range of sizes. 16 The large number of developmental pathways reconstructed by 15 OSA suggests that sequence polymorphism is a widespread as- 14 pect of the postnatal development of these two early theropods. This variation has been interpreted as sexual dimorphism (e.g., Maturity Score 13 ref. 24), but our data do not support this possibility (SI Appendix, 12 Supplementary Text and Fig. S1). The large number of conflicting 11 developmental pathways consisting of semaphoronts with suites 10 of character states that preclude their belonging in other de- 9 velopmental pathways strongly suggests that variation in the 8 relative order of these developmental characters is widespread 7 throughout the populations of these early dinosaurs. Future histological analyses may help to determine whether this lack of 6 correspondence between size and morphological maturity is an 5 expression of how body size is related to ontogenetic age, and 4 although these analyses are outside the scope of the current 3 study, histological data were unhelpful in resolving
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