Phylogenetic Distribution of Extant Richness Suggests Metamorphosis Is a Key Innovation Driving Diversification in Insects

Abstract

Insects and their six-legged relatives (Hexapoda) comprise more than half of all described species and dominate terrestrial and freshwater ecosystems. Understanding the macroevolutionary processes generating this richness requires a historical perspective, but the fossil record of hexapods is patchy and incomplete. Dated molecular phylogenies provide an alternative perspective on divergence times and have been combined with birth-death models to infer patterns of diversification across a range of taxonomic groups. Here we generate a dated phylogeny of hexapod families, based on previously published sequence data and literature derived constraints, in order to identify the broad pattern of macroevolutionary changes responsible for the composition of the extant hexapod fauna. The most prominent increase in diversification identified is associated with the origin of complete metamorphosis, confirming this as a key innovation in promoting insect diversity. Subsequent reductions are recovered for several groups previously identified as having a higher fossil diversity during the Mesozoic. In addition, a number of recently derived taxa are found to have radiated following the development of flowering plant (angiosperm) floras during the mid-Cretaceous. These results reveal that the composition of the modern hexapod fauna is a product of a key developmental innovation, combined with multiple and varied evolutionary responses to environmental changes from the mid Cretaceous floral transition onward.

The fossil record and macroevolutionary history of the beetles

“…This is followed by consistently low levels of extinction throughout the remainder of their history. Similar changes in rates of extinction have also been demonstrated in some other insect clades, with ancient groups having higher extinction rates earlier in their history, followed by lower extinction rates and low richness today [53]. By contrast, very few polyphagan families have gone extinct, so the extinction rate of Polyphaga is always effectively zero (figure 4d).…”

Diversification rates and species richness across the Tree of Life

“…90% in molluscs). Herbivory is demonstrably important for insect diversification [36,37], and complete metamorphosis and wings may also be important [37][38][39]. Furthermore, climatic distribution may be important in explaining patterns of diversification among families within clades (e.g.…”

The microRNA toolkit of insects

“…It is surprising that the emergence of the endopterygotes, the most successful group of metazoans on Earth in terms of diversity33, entailed the appearance of only three microRNAs: Mir-989, Mir-1006 and Mir-1007. One of the more derived features of this subclass and possibly the most influential for diversification, is the holometabolan mode of metamorphosis34, which implies key developmental divergences in the embryo stage8. Thus, further efforts to identify miRNAs in the embryo of holometabolan species should possibly increase the number of specific endopterygote miRNAs.…”