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（stabilizing selection）的塑造，以匹配功能模式。然而，功能交互实际在多大程度上塑造适合度景观（fitness landscape），仍是一个悬而未决的问题。我们以无尾两栖动物（anuran）头骨作为复杂表型的研究模型，借此可区分发育模块化（developmental modularity）与功能模块化（functional modularity）。我们提出假说：与成体头骨功能需求相关的功能模块化，将凌驾于与幼体阶段骨起源（bone origin）相关的发育模块化之上，因为变态发育（metamorphosis）会抹去发育相关的信号。我们利用格拉努莱萨蟾蜍（Rhinella granulosa）复合群的蟾蜍物种，通过物种的表型相关矩阵（P-matrices）对该假说进行了检验。鉴于该类蟾蜍分布于差异显著的生境，且头骨功能与气候条件密切相关，我们还提出另一假说：不同物种间头骨性状协方差模式的差异，与其所处气候变量（climatic variables）的差异存在关联。仅当物种的P矩阵保留尺寸变异信息时，受功能与激素调控的模块才会比发育模块更为显著。若去除尺寸变异，则可清晰观测到发育单元的模块化信号；但在排除异速生长尺寸变异（allometric size variation）的经验数据中，绝大多数物种的最优支持模型为功能模式。亲缘关系较近的蟾蜍物种，其气候生态位（climatic niches）与P矩阵均较远缘物种更为相似，这暗示了系统发育生态位保守性（phylogenetic niche conservatism）。我们推断，源于骨骼胚胎起源的模块化信号（该信号在个体发育（ontogeny）早期即出现），会被个体发育后期的生长过程所掩盖。我们提出，偏好不同模块化模型的物种，其眼眶功能单元的需求存在差异；而气候特征存在显著差异的物种，则受到与神经颅异速生长（neurocranial allometry）及三碘甲状腺原氨酸（T3）激素调控相关的趋异自然选择模式的作用。