Evolvability in the Cephalothoracic Structural Complexity of Aegla araucaniensis (Crustacea: Decapoda) Determined by a Developmental System with Low Covariational Constraint

SIMPLE SUMMARY: The origin of complex morphological structures is explained mainly by direct pathways fusing adjacent modules, while the independent effect of parallel pathways acting on different areas of a morphogenetic field is less well-known. The palimpsest model that explains the cephalothoracic structural complexity of decapod crustaceans is composed of two hox-regulatory parallel pathways that tagmatize the anterior metameres early, followed by a direct pathway that fuses the tagmata forming the developmental modules. The cephalothoracic geometry of Aegla araucaniensis shows a marked sexual dimorphism; its adaptive causes also promote dimorphic variations in the evolvability of developmental modularity. We found areas of instability in the variance of the asymmetry in both developmental modules. The direct pathway presents intermediate levels of canalization in the covariation of the developmental modules, although significantly higher in males. This low restrictive potential promotes expressions of gonadic modularity in females and agonistic modularity in males, which differ significantly from developmental modularity. The cephalothoracic palimpsest model of decapods allows studying modularity in an explicit evo–devo context. ABSTRACT: The integration of complex structures is proportional to the intensity of the structural fusion; its consequences are better known than the covariational effects under less restrictive mechanisms. The synthesis of a palimpsest model based on two early parallel pathways and a later direct pathway explains the cephalothoracic complexity of decapod crustaceans. Using this model, we tested the evolvability of the developmental modularity in Aegla araucaniensis, an anomuran crab with an evident adaptive sexual dimorphism. The asymmetric patterns found on the landmark configurations suggest independent perturbations of the parallel pathways in each module and a stable asymmetry variance near the fusion by canalization of the direct pathway, which was more intense in males. The greater covariational flexibility imposed by the parallel pathways promotes the expression of gonadic modularity that favors the reproductive output in females and agonistic modularity that contributes to mating success in males. Under these divergent expressions of evolvability, the smaller difference between developmental modularity and agonistic modularity in males suggests higher levels of canalization due to a relatively more intense structural fusion. We conclude that: (1) the cephalothorax of A. araucaniensis is an evolvable structure, where parallel pathways promote sexual disruptions in the expressions of functional modularity, which are more restricted in males, and (2) the cephalothoracic palimpsest of decapods has empirical advantages in studying the developmental causes of evolution of complex structures.