Modularity patterns in mammalian domestication: Assessing developmental hypotheses for diversification

Abstract

The neural crest hypothesis posits that selection for tameness resulted in mild alterations to neural crest cells during embryonic development, which directly or indirectly caused the appearance of traits associated with the "domestication syndrome" (DS). Although representing an appealing unitary explanation for the generation of domestic phenotypes, support for this hypothesis from morphological data and for the validity of the DS remains a topic of debate. This study used the frameworks of morphological integration and modularity to assess patterns that concern the embryonic origin of the skull and issues around the neural crest hypothesis. Geometric morphometric landmarks were used to quantify cranial trait interactions between six pairs of wild and domestic mammals, comprising representatives that express between five and 17 of the traits included in the DS, and examples from each of the pathways by which animals entered into relationships with humans. We predicted the presence of neural crest vs mesoderm modular structure to the cranium, and that elements in the neural crest module would show lower magnitudes of integration and higher disparity in domestic forms compared to wild forms. Our findings support modular structuring based on tissue origin (neural crest, mesoderm) modules, along with low module integration magnitudes for neural crest cell derived cranial elements, suggesting differential capacity for evolutionary response among those elements. Covariation between the neural crest and mesoderm modules accounted for major components of shape variation for most domestic/wild pairs. Contra to our predictions, however, we find domesticates share similar integration magnitudes to their wild progenitors, indicating that higher disparity in domesticates is not associated with magnitude changes to integration among either neural crest or mesoderm derived elements. Differences in integration magnitude among neural crest and mesoderm elements across species suggest that developmental evolution preserves a framework that promotes flexibility under the selection regimes of domestication.