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Evolutionary Integration of the Frog Cranium

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Evolutionary Integration of the Frog Cranium ORIGINAL ARTICLE doi:10.1111/evo.13984 Evolutionary integration of the frog cranium Carla Bardua,1,2,3 Anne-Claire Fabre,4 Margot Bon,4 Kalpana Das,5 Edward L. Stanley,6 David C. Blackburn,7 and Anjali Goswami4 1Department of Genetics, Evolution, and Environment, University College London, London , WC1E 6BT, United Kingdom 2Department of Life Sciences, Natural History Museum, London , SW7 5BD, United Kingdom 3E-mail: [email protected] 4Department of Life Sciences, Natural History Museum, London , SW7 5BD, United Kingdom 5Museum für Naturkunde, Leibniz-Institut für Evolutions- und Biodiversitätsforschung, Berlin 10115, Germany 6Department of Herpetology, Florida Museum of Natural History, University of Florida, Gainesville, Florida 32610 7Department of Natural History, Florida Museum of Natural History, University of Florida, Gainesville, Florida 32611 Received September 10, 2019 Accepted April 17, 2020 Evolutionary integration (covariation) of traits has long fascinated biologists because of its potential to elucidate factors that have shaped morphological evolution. Studies of tetrapod crania have identified patterns of evolutionary integration that reflect functional or developmental interactions among traits, but no studies to date have sampled widely across the species-rich lissam- phibian order Anura (frogs). Frogs exhibit a vast range of cranial morphologies, life history strategies, and ecologies. Here, using high-density morphometrics we capture cranial morphology for 172 anuran species, sampling every extant family. We quantify the pattern of evolutionary modularity in the frog skull and compare patterns in taxa with different life history modes. Evolutionary changes across the anuran cranium are highly modular, with a well-integrated “suspensorium” involved in feeding. This pattern is strikingly similar to that identified for caecilian and salamander crania, suggesting replication of patterns of evolutionary integra- tion across Lissamphibia. Surprisingly, possession of a feeding larval stage has no notable influence on cranial integration across frogs. However, late-ossifying bones exhibit higher integration than early-ossifying bones. Finally, anuran cranial modules show diverse morphological disparities, supporting the hypothesis that modular variation allows mosaic evolution of the cranium, but we find no consistent relationship between degree of within-module integration and disparity. KEY WORDS: Frogs, cranial morphology, integration, development, morphometrics, disparity. Trait integration is an inherent property of biological systems and been suggested to promote the diversification of form. Several manifests at many scales of analysis, from populations to large recent studies have explored this hypothesized relationship by clades. Correlations among traits, and their organization into quantifying phenotypic (or variational) and evolutionary integra- highly integrated, semi-autonomous modules, can result from ge- tion and modularity and determining how they relate to disparity netic, developmental, or functional interactions, and it is thought and rates of evolution in various species or clades. These studies that patterns of genetic and developmental integration may provide extensive evidence that the presence of evolutionary evolve adaptively to promote functional integration (Riedl 1978; modules is associated with higher disparity or evolutionary Cheverud 1984; Wagner and Altenberg 1996). These trait associ- rate (Goswami and Polly 2010; Claverie and Patek 2013; Randau ations may be replicated in macroevolutionary patterns observed and Goswami 2017; Felice and Goswami 2018; Larouche et al. across larger clades, with traits evolving in either a coordinated 2018; Dellinger et al. 2019; Watanabe et al. 2019; Bardua et al. or a modular fashion. The modular organization of phenotypic 2019b). Many studies have also assessed whether the magnitude evolution is central to many fundamental concepts in evolution- of evolutionary integration among traits (across an entire pheno- ary biology, including mosaicism (De Beer 1954), which have type or within a module) correlates with higher or lower disparity © 2020 The Authors. Evolution published by Wiley Periodicals LLC on behalf of The Society for the Study of Evolution 1200 This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Evolution 74-6: 1200–1215 FROG CRANIAL INTEGRATION or evolutionary rate. For this question, the answer is less clear tadpoles and frogs can evolve independently, responding to an- than for the one above. Some studies find that high evolutionary tagonistic selection pressures (Sherratt et al. 2017), and different integration among traits is correlated with low disparity and slow tadpole morphologies can converge to the same adult morphol- evolutionary rate (Claverie and Patek 2013; Felice and Goswami ogy (Bragg and Bragg 1958; Pfennig 1990). Frogs with a free- 2018; Martín-Serra et al. 2019). Conversely, others have found living, feeding larval stage may therefore experience fewer de- that highly integrated traits show greater disparity than less velopmental or genetic constraints, which may lead to a decrease integrated ones. In addition, some have found that there is no in strength of phenotypic integration and a greater partitioning of relationship between evolutionary modularity and disparity or traits into modules, or to greater variation in patterns of pheno- rate of evolution at this scale (Goswami et al. 2014; Watanabe typic integration across taxa, both of which would be reflected et al. 2019; Bardua et al. 2019b). However, our understanding in greater evolutionary modularity. Some support for this hypoth- of the factors shaping the evolutionary integration among traits esis is offered by recent analysis of evolutionary modularity in and its relevance for morphological evolution is incomplete, salamanders, with species undergoing complete metamorphosis with most studies focused on a few clades, such as mammals exhibiting elevated cranial modularity compared with pedomor- and birds, both of which have relatively little developmental phic taxa (Fabre et al., 2020). Life history may therefore have diversity. Here, we have expanded the study of evolutionary a significant and persistent influence on the strength and pattern modularity to one of the most taxonomically, developmentally, of cranial integration, and this effect is expected to be particu- ecologically, and morphologically diverse clades of tetrapods: larly strong in lineages with disparate free-living developmental the lissamphibian order Anura (frogs). stages, such as frogs. Lissamphibians constitute over 25% of extant tetrapod Other aspects of development may also influence evolu- species (totalling 8,160 species; AmphibiaWeb 2020), and yet tionary integration across frogs. For example, derivation from patterns of trait integration at any scale across this diverse clade different cranial neural crest (CNC) streams may generate remain largely unexplored compared to amniotes. Previous stud- developmental modules that may be expected to evolve in a ies of both phenotypic and evolutionary integration in lissam- coordinated manner (Felice and Goswami 2018). The pattern phibian crania have found limited support for modular structure, of the contribution of CNC streams to the osteocranium is with studies recovering either few modules or no modular struc- considerably different for the frog Xenopus than for the axolotl (a ture at all (Ivanovic´ and Kalezic´ 2010; Sherratt 2011; Ivanovic´ salamander) or for amniotes (Hanken and Gross 2005; Gross and and Arntzen 2014; Simon and Marroig 2017; Vidal-García and Hanken 2008; Piekarski et al. 2014), suggesting a possible deep Keogh 2017). With the application of high-dimensional geomet- divergence in the pattern of cranial development between frogs ric morphometric data, strong modular structure has been iden- and other tetrapod clades. Furthermore, frogs differ from other tified at the intraspecific (phenotypic) and evolutionary levels lissamphibian clades in cranial ossification sequence timing, across caecilian (Marshall et al. 2019; Bardua et al. 2019b) and with a heterochronic shift whereby frogs exhibit relatively later salamander (Bon et al. 2020; Fabre et al. 2020) crania, in analyses ossification of bones associated with adult feeding (Harrington exploring much wider ranges of models. However, the most di- et al. 2013). Larval and adult feeding modes differ more for frogs verse lissamphibians, frogs, have not yet been incorporated into than for salamanders or caecilians, so larval frog mouthparts these studies. The few studies of cranial modularity in frogs to would likely be more impeded by early ossification of bones in- date vary widely in taxonomic and morphological coverage as volved in adult feeding. However, direct-developing frogs, which well as data type, hindering our understanding of anuran cranial feed like adults immediately following hatching, partially reverse modularity and preventing direct comparison of modular struc- this trend (Hanken et al. 1992; Kerney et al. 2007; Harrington tures across Lissamphibia (e.g., Simon and Marroig 2017; Vidal- et al. 2013). Cranial ossification sequences therefore vary across García and Keogh 2017). Beyond their taxonomic diversity, anu- Anura (Weisbecker and Mitgutsch 2010), and can even vary rans provide a unique opportunity
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