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.形态整合与模块化理论（morphological integration and modularity）预测：若性状间的功能关联与种群平均适合度相关，则发育的遗传基础将经由稳定选择塑造，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，仍是一个悬而未决的问题。我们以无尾两栖类（anuran）头骨作为复杂表型模型，可在此模型中分离发育模块化与功能模块化。我们提出假说：与成体头骨功能需求相关的功能模块化，将超越与幼体阶段骨起源相关的发育模块化，因为变态发育会抹去发育信号。我们利用格拉努莱蟾蜍（Rhinella granulosa）复合群的蟾蜍物种，通过物种表型关联模式（P-矩阵，P-matrices）检验了这一假说。鉴于该蟾蜍类群分布于迥异的生境，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，与各物种间的气候变量差异相关联。仅当物种P-矩阵中保留体型变异时，受功能与激素调控的模块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清晰显现；但在排除异速体型变异（allometric size variation）的经验数据中，多数物种的最优支持模型为功能模块。相较于远缘物种，近缘蟾蜍物种拥有更为相似的气候生态位与P-矩阵，这暗示了系统发育生态位保守性（phylogenetic niche conservatism）。我们推断：胚胎时期骨起源所带来的模块化信号（该信号在个体发育早期出现），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；而气候特征迥异的物种，则受到与神经颅异速生长及T3激素调控相关的自然选择模式的分化作用。