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

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.形态整合与模块化（morphological integration and modularity）理论预测，若性状间的功能关联与种群平均适合度相关，发育的遗传基础将受到稳定选择的塑造，以匹配功能模式。然而，功能交互作用实际在多大程度上塑造适合度景观，仍是一个悬而未决的科学问题。我们以无尾类头骨（anuran skull）作为复杂表型的研究模型，借此可分离发育模块化与功能模块化。我们提出假说：与幼体阶段骨骼胚胎起源相关的发育模块化，会被成体头骨的功能需求所关联的功能模块化超越，因为变态发育会抹去发育信号。我们基于格氏蟾蜍复合种（Rhinella granulosa complex）的表型相关模式（P矩阵，P-matrices）对该假说进行了检验。鉴于该类蟾蜍分布于截然不同的生境，且头骨功能与气候条件密切相关，我们还提出另一假说：不同物种间的头骨性状协变模式差异，与各物种的气候变量差异相关联。仅当物种的P矩阵保留异速生长体型变异时，功能与激素调控模块（functional and hormonal-regulated modules）才会比发育模块更为显著。若剔除体型变异，发育单元的模块化信号会十分清晰，但在不考虑异速生长体型变异的情况下，多数物种的功能模型得到了经验数据的最优支持。亲缘关系较近的蟾蜍物种，其气候生态位与P矩阵均比远缘物种更为相似，这暗示了系统发育生态位保守性（phylogenetic niche conservatism）。我们推断，发生于个体发育早期的骨骼胚胎起源相关的模块化信号，会被个体发育后期的生长过程所模糊。我们认为，偏好不同模块化模型的物种，其眼眶功能单元（orbital functional unit）的需求存在差异；而气候特征不同的物种，则受到与神经颅异速生长（neurocranial allometry）及三碘甲状腺原氨酸（T3）激素调控相关的自然选择压力的分化作用。