Evolution of a complex phenotype with biphasic ontogeny: Contribution of development versus function and climatic variation to skull modularity in toads

Abstract

The theory of morphological integration and modularity predicts that if functional correlations among traits are relevant to mean population fitness, the genetic basis of development will be molded by stabilizing selection to match functional patterns. Yet, how much functional interactions actually shape the fitness landscape is still an open question. We used the anuran skull as a model of a complex phenotype for which we can separate developmental and functional modularity. We hypothesized that functional modularity associated to functional demands of the adult skull would overcome developmental modularity associated to bone origin at the larval phase because metamorphosis would erase the developmental signal. We tested this hypothesis in toad species of the Rhinella granulosa complex using species phenotypic correlation pattern (P‐matrices). Given that the toad species are distributed in very distinct habitats and the skull has important functions related to climatic conditions, we also hypothesized that differences in skull trait covariance pattern are associated to differences in climatic variables among species. Functional and hormonal‐regulated modules are more conspicuous than developmental modules only when size variation is retained on species P‐matrices. Without size variation, there is a clear modularity signal of developmental units, but most species have the functional model as the best supported by empirical data without allometric size variation. Closely related toad species have more similar climatic niches and P‐matrices than distantly related species, suggesting phylogenetic niche conservatism. We infer that the modularity signal due to embryonic origin of bones, which happens early in ontogeny, is blurred by the process of growth that occurs later in ontogeny. We suggest that the species differing in the preferred modularity model have different demands on the orbital functional unit and that species contrasting in climate are subjected to divergent patterns of natural selection associated to neurocranial allometry and T3 hormone regulation.

Evolutionary integration of the frog cranium

“…We find anuran crania evolve in a highly modular manner, exhibiting 13 distinct evolutionary modules. Our results contrast with previous analyses recovering only weak support for phenotypic or evolutionary modularity across frog crania (Simon and Marroig 2017; Vidal‐García and Keogh 2017), and we find no support for the functional models investigated in these studies. However, those studies investigated modularity at a finer taxonomic scale, sampling at subgenus or family level, respectively, with likely greater similarity (and less variation) in function and ecology than is sampled here.…”

“…We hypothesized 27 different model structures, ranging from a fully integrated cranium (one “module”), to every bone or every region as its own module (14 or 19 modules) (see Table 1). We compared a range of models based on function, development, and ossification sequence rank, including models modified from previous studies (Simon and Marroig 2017; Vidal‐García and Keogh 2017). These include models based on the contribution of CNC streams to cranial bones, and various divisions of the cranium based on hypothesized functional units.…”

Postmetamorphic ontogenetic allometry and the evolution of skull shape in Nest‐building frogs Leptodactylus (Anura: Leptodactylidae)

“…On the other hand, macroevolutionary allometric patterns as related to cranial interspecific variation were studied in amphibians and other groups of tetrapods (Esquerré, Sherratt, & Keogh, 2017;Ivanović & Arntzen, 2014Klingenberg & Marugán-Lobón, 2013;Openshaw & Keogh, 2014;Sherratt, Gower, Klingenberg, & Wilkinson, 2014;Tavares, Pessôa, & Seuánez, 2016;Wilson, 2013;Wilson & Sánchez Villagra, 2011). Particularly in anurans, several authors have addressed large-scale studies about skull morphological diversification (e.g., Emerson, 1985;Simon & Marroig, 2017;Simon, Machado, & Marroig, 2016;Yeh, 2002a), but to our knowledge, patterns of postmetamorphic skull development and their relationship with diversity in adult morphology have been explored in a few clades (Fabrezi, 2006;Fabrezi et al, 2016;Ponssa & Vera Candioti, 2012;Yeh, 2002b).…”

Copulatory function and development shape modular architecture of genitalia differently in males and females

“…Developmental integration is likely to be a major constraint to phenotypic evolution (Punzalan and Rowe 2016; Simon and Marroig 2017), especially if persistent stabilizing selection associated to development counteracts directional selection. In contrast, the combination of stabilizing and divergent directional selection (i.e., selection in opposite directions on sets of traits) presents the ideal scenario for the maintenance of modularity (Melo and Marroig 2015).…”

“…An intriguing example is the dragonfly wing, where different areas responsible for wing folding during flight represent a functional module (Blanke 2018). Interestingly, if there is a mismatch between function and development, that is, groups of structures that work together are different from groups that share a unique developmental origin, it becomes possible to test which of these two factors is more determinant to trait covariation (Simon and Marroig 2017). To date, there is not a consensus on which of these forms of interaction, if any, is more determinant to trait modularity.…”