Diversification dynamics of hypermetamorphic blister beetles (Meloidae): Are homoplastic host shifts and phoresy key factors of a rushing forward strategy to escape extinction?

Abstract

Changes in life history traits, including reproductive strategies or host shifts, are often considered triggers of speciation, affecting diversification rates. Subsequently, these shifts can have dramatic effects on the evolutionary history of a lineage. In this study, we examine the consequences of changes in life history traits, in particular host-type and phoresy, within the hypermetamorphic clade of blister beetles (Meloidae). This clade exhibits a complex life cycle involving multiple metamorphoses and parasitoidism. Most tribes within the clade are bee-parasitoids, phoretic or non-phoretic, while two tribes feed on grasshopper eggs. Species richness differs greatly between bee and grasshopper specialist clades, and between phoretic and non-phoretic genera. We generated a mitogenomic phylogeny of the hypermetamorphic clade of Meloidae, including 21 newly generated complete mitogenomes. The phylogeny and estimated lineage divergence times were used to explore the association between diversification rates and changes in host specificity and phoresy, using State-Dependent Speciation and Extinction (SSE) models, while accounting for hidden factors and phylogenetic uncertainty within a Bayesian framework. The ancestor of the hypermetamorphic Meloidae was a non-phoretic bee-parasitoid, and independent transitions towards phoretic bee-parasitoidism or grasshopper specialization occurred multiple times. Bee-parasitoid lineages that are non-phoretic have significantly higher relative extinction rates and lower diversification rates than grasshopper specialists or phoretic bee-parasitoids, while no significant differences were found between the latter two strategies. This suggests that these two life strategies contributed independently to the evolutionary success of Nemognathinae and Meloinae, allowing them to escape from the evolutionary constraints imposed by their hypermetamorphic life-cycle, and that the "bee-by-crawling" strategy may be an evolutionary "dead end". We show how SSE models can be used not only for testing diversification dependence in relation to the focal character but to identify hidden traits contributing to the diversification dynamics. The ability of blister beetles to explore new evolutionary scenarios including the development of homoplastic life strategies, are extraordinary outcomes along the evolution of a single lineage: the hypermetamorphic Meloidae.