Modularity, evolvability, and adaptive radiations: a comparison of the hemi‐ and holometabolous insects

Abstract

Despite recent attention given to the concept of modularity and its potential contribution to the evolvability of organisms, there has been little mention of how such a contribution may affect rates of diversification or how this would be assessed. A first key prediction is that lineages with relatively greater degrees of modularity in given traits should exhibit higher rates of diversification. Four general conditions for testing this prediction of the modular evolvability hypothesis are outlined here. The potential role of modularity as a deterministic factor in adaptive radiations is best examined by looking at historic patterns of diversification rather than just levels of extant diversity, the focus of most analyses of key innovations. Recent developmental evidence supports the notion that phenotypes of juvenile and adult stages of insects with "complete" metamorphosis (Holometabola) are distinct developmental and evolvable modules compared to the highly correlated life stages of insects with "incomplete" metamorphosis (Hemimetabola). Family-level rates of diversification for these two groups were calculated from the fossil record. The Holometabola was found to have a significantly and characteristically higher rate of diversification compared to the less modular Hemimetabola, consistent with the idea that intrinsic differences in modularity can influence the long-term evolvability of organisms. The modular evolvability hypothesis also makes a second key prediction: that characters in more modular clades will exhibit greater levels of variation due to their independence. This provides an independent, phenotypically based test of the hypothesis. We discuss here how this second prediction may be tested in the case of the Hemi- and Holometabola.

Fossil evidence for key innovations in the evolution of insect diversity

“…These facts, long casually observed, have suggested that key evolutionary changes have been responsible for generating much of the richness in this very diverse group, and four such evolutionary innovations have held centre stage [18,19]: the insect bauplan [35], wings [36], wing folding [21] and complete metamorphosis [23]. Here, we have reported evidence that both fossil family rspb.royalsocietypublishing.org Proc.…”

“…[11]). Fossil studies have been rare, but Yang [23] used Lyellian survival analysis on family-level data [24] to suggest that extinction rates do not differ between Holometabola and Paraneoptera, and hence that differences in origination rates probably account for the larger increase in families in Holometabola. However, Yang only considered this single key innovation, and the dataset on which his study was based is now considerably dated.…”

Adaptive response to sociality and ecology drives the diversification of facial colour patterns in catarrhines

“…The evolution of higher facial colour complexity within genera indicates de-coupling of the phenotype of different facial regions, which is consistent with the idea that these might constitute variational modules 10 . Modularity of the primate face is a likely advantage of these more structured facial colour patterns because it can enable higher levels of interspecific diversity 10,36,37 that would in turn be beneficial for species recognition. A modular framework characterizes the cranial morphology of many mammals, including primates [38][39][40] ; however, facial colour patterns have not been investigated in the context of modularity even though research suggests that various aspects of this system might be modular.…”

Evidence for an Earliest Late Carboniferous Divergence Time and the Early Larval Ecology and Diversification of Major Holometabola Lineages

“…But their permanent establishment would have been assured only after the emptying of ecological space after the end-Permian event. It is this profound, postPermian ecological transformation that provided a sufficient number of available niches that allowed permanent establishment of several major clades with complete metamorphosis (Yang, 2001;Mayhew, 2002Mayhew, , 2007. This suggests that holometaboly was initially important in species-byspecies replacement of nonholometabolous taxa resulting from Permian climatic vicissitude that only later was implemented during the Triassic when a different process of niche reorganization allowed occupation.…”