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Morphological Evolution and Modularity of the Caecilian Skull Carla Bardua1,2* , Mark Wilkinson1, David J

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Morphological Evolution and Modularity of the Caecilian Skull Carla Bardua1,2* , Mark Wilkinson1, David J Bardua et al. BMC Evolutionary Biology (2019) 19:30 https://doi.org/10.1186/s12862-018-1342-7 RESEARCH ARTICLE Open Access Morphological evolution and modularity of the caecilian skull Carla Bardua1,2* , Mark Wilkinson1, David J. Gower1, Emma Sherratt3 and Anjali Goswami1,2 Abstract Background: Caecilians (Gymnophiona) are the least speciose extant lissamphibian order, yet living forms capture approximately 250 million years of evolution since their earliest divergences. This long history is reflected in the broad range of skull morphologies exhibited by this largely fossorial, but developmentally diverse, clade. However, this diversity of form makes quantification of caecilian cranial morphology challenging, with highly variable presence or absence of many structures. Consequently, few studies have examined morphological evolution across caecilians. This extensive variation also raises the question of degree of conservation of cranial modules (semi-autonomous subsets of highly-integrated traits) within this clade, allowing us to assess the importance of modular organisation in shaping morphological evolution. We used an intensive surface geometric morphometric approach to quantify cranial morphological variation across all 32 extant caecilian genera. We defined 16 cranial regions using 53 landmarks and 687 curve and 729 surface sliding semilandmarks. With these unprecedented high-dimensional data, we analysed cranial shape and modularity across caecilians assessing phylogenetic, allometric and ecological influences on cranial evolution, as well as investigating the relationships among integration, evolutionary rate, and morphological disparity. Results: We found highest support for a ten-module model, with greater integration of the posterior skull. Phylogenetic signal was significant (Kmult =0.87,p < 0.01), but stronger in anterior modules, while allometric influences were also significant (R2 =0.16,p < 0.01), but stronger posteriorly. Reproductive strategy and degree of fossoriality were small but significant influences on cranial morphology (R2 =0.03–0.05), after phylogenetic (p <0.03) and multiple-test (p < 0.05) corrections. The quadrate-squamosal ‘cheek’ module was the fastest evolving module, perhaps due to its pivotal role in the unique dual jaw-closing mechanism of caecilians. Highly integrated modules exhibited both high and low disparities, and no relationship was evident between integration and evolutionary rate. Conclusions: Our high-dimensional approach robustly characterises caecilian cranial evolution and demonstrates that caecilian crania are highly modular and that cranial modules are shaped by differential phylogenetic, allometric, and ecological effects. More broadly, and in contrast to recent studies, this work suggests that there is no simple relationship between integration and evolutionary rate or disparity. Keywords: Amphibia, Caecilians, Cranial, Evolution, Evolutionary rate, Gymnophiona, Integration, Macroevolution, Modularity, Skulls * Correspondence: [email protected] 1Department of Life Sciences, Natural History Museum, London, UK 2Department of Genetics, Evolution and Environment, UCL, London, UK Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Bardua et al. BMC Evolutionary Biology (2019) 19:30 Page 2 of 23 Background of the sensory, feeding, respiratory, and communication A thorough understanding of the morphological evolu- systems, the cranium has been shaped by numerous, tion of a clade requires considering both intrinsic (e.g., often competing, demands. The cranium is also develop- developmental) and extrinsic (e.g., environmental) influ- mentally complex, with different embryonic origins ences. Examining morphological evolution through clade (neural crest and paraxial mesoderm) and types of ossifi- history can reveal disparate patterns, from phylogenetic cations (endochondral and intramembranous) across the conservatism (e.g., [1, 2]) to repeated convergent evolu- cranial bones. Previous studies have identified a complex tion through adaptation (e.g., [3–6]) or directional evolu- modular cranial structure in some vertebrate clades, tion [7, 8]. Quantification of these patterns also often reflecting this functional and developmental complexity. further demonstrates that different biological structures, A six-module model has been identified in carnivorans or different parts of structures, may deviate in their [18], macaques [27, 28], and across therians [29], sug- patterns of evolution. Individual structures may have di- gesting this model may be conserved across a range of vergent localised functions or different developmental mammals. Modularity has also been studied across 15 origins and therefore be subject to different constraints. orders of Mammalia [22], and similar patterns of trait However, each structure also contributes to the func- correlations were found, suggesting a common covari- tionality and, ultimately, to the fitness of the whole or- ance structure of the mammalian cranium. Avian crania ganism. For example, multiple levels of functional and have been proposed to have seven distinct modules [19], developmental interactions have been demonstrated with some concordance with mammalian modules within Felidae, from the level of the individual vertebrae (vault, basicranium) as well as some novel modules (e.g., [9], to different vertebral regions [10], to the level of the nares). Several studies have limited analysis to a higher presacral vertebral column [11]. This hierarchy of inter- level division of the neurocranium and facial modules, actions across the presacral vertebral column of felids and this model also has strong support [30, 31]. Previous demonstrates how multiple levels of organisation shape work on cranial modularity has been strongly biased to- the morphological evolution of a complex structure. wards amniotes (especially mammals). In contrast, stud- The complex hierarchy of functional, developmental ies of modularity and integration in non-amniotes or genetical relationships among traits underlies the (amphibians) are rare, limiting our understanding of the concepts of modularity and integration. Integration re- diversity of patterns of modularity and our ability to re- fers to the covariation or correlation amongst traits, construct evolutionary trends in those clades. while modularity refers to the partitioning of highly inte- As the only extant non-amniote tetrapod clade, Lis- grated traits into semi-independent subsets (modules). samphibia (Anura, Caudata and Gymnophiona = frogs Modular structures can be identified as those that can and toads, salamanders and newts, and caecilians, re- be divided into subunits, or modules, that exhibit strong spectively) represents a unique lineage for comparison within-module integration (trait covariation) and weaker with patterns of modularity and integration identified in between-module integration [12–14]. Trait regionalisa- amniote crania. Evolutionary modularity has been ex- tion in modular networks is hypothesized to promote plored in salamander crania using cranial ossification se- evolvability [15], allowing strongly related traits to co- quences, and support was found for two (or four) vary, and coevolve, with relative autonomy from other developmental modules in terms of coordinated timing regions. Strong integration within modules has been of development [32]. However, landmark studies suggest found to facilitate (e.g., [9, 16, 17]), constrain (e.g., [18, salamander crania may be highly integrated, with no dis- 19]) or both facilitate and constrain [20] evolution, af- tinct modules across the cranium of the alpine newt [33] fecting the magnitude and direction of an organismal or the crania of species of Triturus [34]. Modularity has lineage’s response to selection [20–23]. More specifically, also been studied in frogs, by comparing morphological integration directs evolutionary shifts to favoured re- evolution and covariation in limbs and crania across the gions of morphospace, i.e. along paths of least resistance, Myobatrachidae [1], testing alternative two or three- which may promote homoplasy as organismal evolution module models, but finding no strong support for any is directed along similar evolutionary trajectories defined modular structure. Similarly, only weak support was by the underlying architecture of trait interactions [20, found for models of three to five developmental, func- 24, 25]. Identifying the structure of these trait interac- tional and hormonal modules [35] in crania of the tions through quantitative analysis is thus central to ad- anuran Rhinella granulosa complex. In a previous inves- vancing understanding of morphological evolution. tigation, Sherratt [36] found support for a two-module The focus of many studies of phenotypic integration model in caecilian crania, with independence of the and modularity is the vertebrate cranium, a complex snout relative to
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