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The Many Faces of Synapsid Cranial Allometry

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The Many Faces of Synapsid Cranial Allometry Paleobiology, 45(4), 2019, pp. 531–545 DOI: 10.1017/pab.2019.26 Article The many faces of synapsid cranial allometry Isaac W. Krone , Christian F. Kammerer, and Kenneth D. Angielczyk Abstract.—Previous studies of cranial shape have established a consistent interspecific allometric pattern relating the relative lengths of the face and braincase regions of the skull within multiple families of mam- mals. In this interspecific allometry, the facial region of the skull is proportionally longer than the braincase in larger species. The regularity and broad taxonomic occurrence of this allometric pattern suggests that it may have an origin near the base of crown Mammalia, or even deeper in the synapsid or amniote forerun- ners of mammals. To investigate the possible origins of this allometric pattern, we used geometric morpho- metric techniques to analyze cranial shape in 194 species of nonmammalian synapsids, which constitute a set of successive outgroups to Mammalia. We recovered a much greater diversity of allometric patterns within nonmammalian synapsids than has been observed in mammals, including several instances similar to the mammalian pattern. However, we found no evidence of the mammalian pattern within Theroce- phalia and nonmammalian Cynodontia, the synapsids most closely related to mammals. This suggests that the mammalian allometric pattern arose somewhere within Mammaliaformes, rather than within nonmammalian synapsids. Further investigation using an ontogenetic series of the anomodont Diictodon feliceps shows that the pattern of interspecific allometry within anomodonts parallels the ontogenetic trajectory of Diictodon. This indicates that in at least some synapsids, allometric patterns associated with ontogeny may provide a “path of least resistance” for interspecific variation, a mechanism that we suggest produces the interspecific allometric pattern observed in mammals. Isaac W. Krone.* University of Chicago, Chicago, Illinois 60637, U.S.A. E-mail: [email protected].*Present address: Museum of Vertebrate Zoology, University of California, Berkeley, California 94720-3161, U.S.A. Christian F. Kammerer. North Carolina Museum of Natural Sciences, Raleigh, North Carolina 27601-1029, U.S.A. E-mail: [email protected] Kenneth D. Angielczyk. Integrative Research Center, Field Museum of Natural History, 1400 South Lake Shore Drive, Chicago, Illinois 60605-2827, U.S.A. E-mail: kangielczyk@fieldmuseum.org Accepted: 26 July 2019 First published online: 12 September 2019 Data available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.56qq231 Introduction Goswami 2006; Goswami and Polly 2010; The cranium is a highly complex structure Angielczyk and Ruta 2012; Bhullar et al. 2012; that has evolved myriad forms associated Brusatte et al. 2012; Foth and Rauhut 2013; Zel- with many different ecologies throughout the ditch and Calamari 2016), including those with tetrapod radiation. Despite this fact, tetrapod idiosyncratic or highly derived cranial struc- crania all exhibit a shared basic architecture— tures (Claude et al. 2004; Sherratt et al. 2014; a braincase and associated sensory capsules Churchill et al. 2018). However, little work has and a facial skeleton associated with the jaws been done to synthesize the results of these ana- (Emerson and Bramble 1993)—facilitating com- lyses or to look for pan-tetrapod morphological parisons across the group. Many tetrapod patterns. clades also have an extensive fossil record One such pan-tetrapod pattern has been sug- including well-preserved crania. These clades gested, albeit obliquely, by analyses of cranial provide excellent systems in which to study allometry in crown mammals. Within other- both small- and large-scale patterns in shape wise morphologically conservative mamma- evolution over time. Recent large-scale analyses lian families, there exists a widespread pattern of tetrapod crania have used geometric mor- of interspecific allometry in which larger ani- phometric techniques to address questions of mals have proportionately longer faces disparity and allometry within a variety of (Radinsky 1985; Cardini and Polly 2013; major tetrapod groups (e.g., Stayton 2005; Cardini et al. 2015; Cardini 2019). Studies © 2019 The Paleontological Society. All rights reserved. This is an Open Access article, distributed under the terms of the DownloadedCreative from https://www.cambridge.org/core Commons Attribution licence. IP address: (http://creativecommons.org/licenses/by/4.0/), 170.106.35.76, on 24 Sep 2021 at 16:34:59, subject to the Cambridge which permits Core terms unrestricted of use, available at https://www.cambridge.org/core/termsre-use, distribution, and reproduction. https://doi.org/10.1017/pab.2019.26 in any medium, provided the original work is properly cited. 0094-8373/19 532 ISAAC W. KRONE ET AL. using geometric morphometric techniques Outside of mammals, fewer studies have have suggested that this trend is a salient and explicitly focused on large-scale analyses of widespread pattern of cranial allometry within allometry within tetrapod crania. Angielczyk Mammalia, characterizing groups as disparate and Ruta (2012) found a pattern similar to as antelopes (Antilopinae and Cephalopinae), CREA within Permo-Carboniferous temno- fruit bats (Pteropodidae), African mongooses spondyl amphibians. Smaller temnospondyls (Herpestidae), African tree squirrels (Sciuridae) tended to have short, broad snouts, whereas (Cardini and Polly 2013), cats (Felidae) (Tamag- larger temnospondyls had proportionally nini et al. 2017), and kangaroos (Macropodidae) longer snouts. In addition, Bright et al. (2016) (Cardini et al. 2015; but see Mitchell et al. 2018). and Linde-Medina (2016) recovered CREA-like Cardini et al. (2015) referred to this pattern of patterns in raptors and Galliformes, respect- snout length allometry within closely related ively, using geometric morphometric techni- and morphologically conservative groups as ques, though Linde-Medina found a traditional the “cranial rule of evolutionary allometry,” or morphometric approach does not recover a CREA, and suggested that it may be as wide- CREA-like pattern and suggested that the use spread as Bergmann’s rule and Allen’s rule, of centroid size as a predictor variable may be extending to nearly all mammals. problematic. If it is indeed so ubiquitous, the CREA pat- Because temnospondyls, mammals, and tern demands explanation. Cardini and Polly birds represent each of the three great lineages (2013) suggested that the pattern may be driven of crown tetrapods that diverged in the Carbon- by disparity in allometric scaling between the iferous (Benton et al. 2015), it is possible that a body, the jaw, and the brain. Because brain CREA-like allometric pattern is common to all size scales with a ¾ exponent relative to body tetrapods, in line with Cardini and Polly’s mass (Martin et al. 2005), and jaw length (2013) scaling hypothesis. If the similar allomet- (under isometry) should scale with a ⅓ expo- ric patterns in temnospondyls, birds, and mam- nent relative to body mass, the relative length mals reflect an ancestral tetrapod pattern, we of the braincase should scale at a lower rate would expect a CREA-like pattern to character- than the jaw. This produces a pattern of cranial ize nonmammalian synapsids, the now-extinct allometry in which larger animals have rela- members of the mammalian stem lineage. tively longer faces, because the snout must Alternatively, if the CREA pattern is not an grow in line with the jaw to allow effective feed- ancestral tetrapod trait, we predict that other ing. Due to the shared architecture of tetrapod patterns of cranial allometry would be present crania and the difference in growth rate in nonmammalian synapsids, although some between the braincase and the jaw, this explan- synapsids might have evolved a similar allomet- ation, if valid, predicts an extension of the ric relationship independently. The evolution of CREA pattern to all tetrapods. synapsid skull characters is well-studied (e.g., Cardini and Polly (2013) also noted the inter- Kemp 1982, 2005; Hopson 1991; Sidor and Hop- relationship between ontogenetic allometry in son 1998;Sidor2001; Esteve-Altava et al., 2013; mammals and the observed pattern of interspe- Benoit et al. 2016; Angielczyk and Kammerer cific allometry with respect to the relative size of 2018), and the overall trend toward a more the snout. Juvenile mammals generally display mammal-like skull within therapsids offers the a higher degree of brachycephaly compared possibility of pinpointing when this pattern of with adults of the same species, creating an interspecific allometry evolved. ontogenetic pattern that mirrors CREA. They For this study, we assembled a photographic posited that this allometric relationship con- library of lateral-view images of nonmammalian strains the degree to which heterochronic shifts synapsid crania for use in geometric morphomet- in the rate of development of the facial region ric analyses. Our sample includes all major groups can operate to change adult snout length in of “pelycosaur”-grade synapsids (Caseasauria mammals. They also suggested that this link [Eothyrididae + Caseidae], Varanopidae, Ophia- between size and shape allows shape adapta- codontidae, Edaphosauridae, Sphenacodontidae) tion to proceed through changes in body size. and therapsids (Biarmosuchia, Dinocephalia, Downloaded from https://www.cambridge.org/core. IP address: 170.106.35.76, on 24 Sep 2021 at 16:34:59, subject to the Cambridge
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