Phylogenetic Analyses of True Ladybirds (Coleoptera: Coccinellidae: Coccinellini) Reveal Directionality in Diet Evolution and Support a Boreotropical Origin of the Tribe

ABSTRACT True ladybirds (Coleoptera: Coccinellidae: Coccinellini) are an iconic and beloved group of insects comprising c . 1000 species. Contrary to common belief, true ladybirds are not restricted to temperate areas in the Northern hemisphere and can be found on every continent (with the exception of Antarctica). Moreover, although they are commonly viewed as aphid specialists, they actually have a wider range of diets, with some species being, for example, mildew fungus specialists. To better understand their biogeographic history and diet evolution, we generate the current largest dated molecular phylogeny of Coccinellini, based on a multi‐marker molecular dataset (three mitochondrial and eight nuclear gene fragments) for 206 species representing 57 genera, plus 44 outgroups. The resulting phylogenetic hypothesis clarifies the relationships between main clades and genera while providing a more comprehensive framework to draw inferences on the evolution of the tribe. Our historical biogeography analyses reveal a dynamic but highly structured pattern for the tribe, consistent with the hypothesis of a boreotropical origin during the Paleocene. From there, numerous lineages spread southward, with multiple independent colonizations of the Afrotropical, Australasian, and Neotropical regions. Bayesian stochastic mapping analyses also highlight interesting patterns, such as the pivotal role of the East Palearctic region and the importance of Beringian land bridges in the dispersal of lineages toward the Nearctic. Ancestral character state estimation analyses recover a structured pattern, with an ancestral association on aphids often followed by a broadening of the host repertoire and secondary shifts onto different food sources. These analyses also support the existence of a directionality in diet evolution, where expansion of the host repertoire constitutes a prerequisite for shifting to a novel food resource; interestingly, the only marked exception to this pattern is the single shift from aphids to mildew fungi leading to the diversification of a specific mycetophagous lineage.