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Mitogenomics and hidden-trait models reveal the role of phoresy and host shifts in the diversification of parasitoid blister beetles (Coleoptera: Meloidae).

ABSTRACT: Changes in life history traits are often considered speciation triggers and can have dramatic effects on the evolutionary history of a lineage. Here, we examine the consequences of changes in two life history traits, host-type and phoresy, in the hypermetamorphic blister beetles, Meloidae. Subfamilies Nemognathinae and Meloinae exhibit a complex life cycle involving multiple metamorphoses and parasitoidism. Most genera and tribes are bee-parasitoids, and include phoretic or nonphoretic species, while two tribes feed on grasshopper eggs. These different life strategies are coupled with striking differences in species richness among clades. We generated a mitogenomic phylogeny for Nemognathinae and Meloinae, confirming the monophyly of these two clades, and used the dated phylogeny to explore the association between diversification rates and changes in host specificity and phoresy, using state-dependent speciation and extinction (SSE) models that include the effect of hidden traits. To account for the low taxon sampling, we implemented a phylogenetic-taxonomic approach based on birth-death simulations, and used a Bayesian framework to integrate parameter and phylogenetic uncertainty. Results show that the ancestral hypermetamorphic Meloidae was a nonphoretic bee-parasitoid, and that transitions towards a phoretic bee-parasitoid and grasshopper parasitoidism occurred multiple times. Nonphoretic bee-parasitoid lineages exhibit significantly higher relative extinction and lower diversification rates than phoretic bee-and grasshopper-parasitoids, but no significant differences were found between the latter two strategies. This suggests that Orthopteran host shifts and phoresy contributed jointly to the evolutionary success of the parasitoid meloidae. We also demonstrate that SSE models can be used to identify hidden traits coevolving with the focal trait in driving a lineage's diversification dynamics.

SUBMITTER: Lopez-Estrada EK

PROVIDER: S-EPMC9305437 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Insect mitochondrial genomes (mitogenomes) exhibit high diversity in some lineages. The gene rearrangement and large intergenic spacer (IGS) have been reported in several Coleopteran species, although very little is known about mitogenomes of Meloidae.We determined complete or nearly complete mitogenomes of seven meloid species. The circular genomes encode 13 protein-coding genes (PCGs), 22 transfer RNAs (tRNAs) and two ribosomal RNAs (rRNAs), and contain a control region, with gene arrangement identical to the ancestral type for insects. The evolutionary rates of all PCGs indicate that their evolution is based on purifying selection. The comparison of tRNA secondary structures indicates diverse substitution patterns in Meloidae. Remarkably, all mitogenomes of the three studied Hycleus species contain two large intergenic spacers (IGSs). IGS1 is located between trnW and trnC, including a 9 bp consensus motif. IGS2 is located between trnS2 (UCN) and nad1, containing discontinuous repeats of a pentanucleotide motif and two 18-bp repeat units in both ends. To date, IGS2 is found only in genera Hycleus across all published Coleopteran mitogenomes. The duplication/random loss model and slipped-strand mispairing are proposed as evolutionary mechanisms for the two IGSs (IGS1, IGS2). The phylogenetic analyses using MrBayes, RAxML, and PhyloBayes methods based on nucleotide and amino acid datasets of 13 PCGs from all published mitogenomes of Tenebrionoids, consistently recover the monophylies of Meloidae and Tenebrionidae. Within Meloidae, the genus Lytta clusters with Epicauta rather than with Mylabris. Although data collected thus far could not resolve the phylogenetic relationships within Meloidae, this study will assist in future mapping of the Meloidae phylogeny.This study presents mitogenomes of seven meloid beetles. New mitogenomes retain the genomic architecture of the Coleopteran ancestor, but contain two IGSs in the three studied Hycleus species. Comparative analyses of two IGSs suggest that their evolutionary mechanisms are duplication/random loss model and slipped-strand mispairing.

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Mitogenomics and hidden-trait models reveal the role of phoresy and host shifts in the diversification of parasitoid blister beetles (Coleoptera: Meloidae).

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