Phylogenomics of Ichneumonoidea (Hymenoptera) and implications for evolution of mode of parasitism and viral endogenization.

Ichneumonoidea is one of the most diverse lineages of animals on the planet with >48,000 described species and many more undescribed. Parasitoid wasps of this superfamily are mostly beneficial insects that attack and kill other arthropods and are important for understanding diversification and the evolution of life history strategies related to parasitoidism. Further, some lineages of parasitoids within Ichneumonoidea have acquired endogenous virus elements (EVEs) that are permanently a part of the wasp's genome and benefit the wasp through host immune disruption and behavioral control. Unfortunately, understanding the evolution of viral acquisition, parasitism strategies, diversification, and host immune disruption mechanisms, is deeply limited by the lack of a robust phylogenetic framework for Ichneumonoidea. Here we design probes targeting 541 genes across 91 taxa to test phylogenetic relationships, the evolution of parasitoid strategies, and the utility of probes to capture polydnavirus genes across a diverse array of taxa. Phylogenetic relationships among Ichneumonoidea were largely well resolved with most higher-level relationships maximally supported. We noted codon use biases between the outgroups, Braconidae, and Ichneumonidae and within Pimplinae, which were largely solved through analyses of amino acids rather than nucleotide data. These biases may impact phylogenetic reconstruction and caution for outgroup selection is recommended. Ancestral state reconstructions were variable for Braconidae across analyses, but consistent for reconstruction of idiobiosis/koinobiosis in Ichneumonidae. The data suggest many transitions between parasitoid life history traits across the whole superfamily. The two subfamilies within Ichneumonidae that have polydnaviruses are supported as distantly related, providing strong evidence for two independent acquisitions of ichnoviruses. Polydnavirus capture using our designed probes was only partially successful and suggests that more targeted approaches would be needed for this strategy to be effective for surveying taxa for these viral genes. In total, these data provide a robust framework for the evolution of Ichneumonoidea.

Phylogenomic Evidence Overturns Current Conceptions of Social Evolution in Wasps (Vespidae).

The hypothesis that eusociality originated once in Vespidae has shaped interpretation of social evolution for decades and has driven the supposition that preimaginal morphophysiological differences between castes were absent at the outset of eusociality. Many researchers also consider casteless nest-sharing an antecedent to eusociality. Together, these ideas endorse a stepwise progression of social evolution in wasps (solitary → casteless nest-sharing → eusociality with rudimentary behavioral castes → eusociality with preimaginal caste-biasing (PCB) → morphologically differentiated castes). Here, we infer the phylogeny of Vespidae using sequence data generated via anchored hybrid enrichment from 378 loci across 136 vespid species and perform ancestral state reconstructions to test whether rudimentary and monomorphic castes characterized the initial stages of eusocial evolution. Our results reject the single origin of eusociality hypothesis, contest the supposition that eusociality emerged from a casteless nest-sharing ancestor, and suggest that eusociality in Polistinae + Vespinae began with castes having morphological differences. An abrupt appearance of castes with ontogenetically established morphophysiological differences conflicts with the current conception of stepwise social evolution and suggests that the climb up the ladder of sociality does not occur through sequential mutation. Phenotypic plasticity and standing genetic variation could explain how cooperative brood care evolved in concert with nest-sharing and how morphologically dissimilar castes arose without a rudimentary intermediate. Furthermore, PCB at the outset of eusociality implicates a subsocial route to eusociality in Polistinae + Vespinae, emphasizing the role of mother-daughter interactions and subfertility (i.e. the cost component of kin selection) in the origin of workers.

Conditional indirect genetic effects of caregivers on brood in the clonal raider ant.

Caregivers shape the rearing environment of their young. Consequently, offspring traits are influenced by the genes of their caregivers via indirect genetic effects (IGEs). However, the extent to which IGEs are modulated by environmental factors, other than the genotype of social partners (i.e., intergenomic epistasis), remains an open question. Here we investigate how brood are influenced by the genotype of their caregivers in the clonal raider ant, Ooceraea biroi, a species in which the genotype, age and number of both caregivers and brood can be experimentally controlled. First, we used four clonal lines to establish colonies that differed only in the genotype of caregivers and measured effects on foraging activity, as well as IGEs on brood phenotypes. In a second experiment, we tested whether these IGEs are conditional on the age and number of caregivers. We found that caregiver genotype affected the feeding and foraging activity of colonies, and influenced the rate of development, survival, body size, and caste fate of brood. Caregiver genotype interacted with other factors to influence the rate of development and survival of brood, demonstrating that IGEs can be conditional. Thus, we provide an empirical example of phenotypes being influenced by IGE-by-environment interactions beyond intergenomic epistasis, highlighting that IGEs of caregivers/parents are alterable by factors other than their brood's/offspring's genotype.

Transcriptional and post-transcriptional control of odorant receptor choice in ants.

Insects and mammals have independently evolved odorant receptor genes that are arranged in large genomic tandem arrays. In mammals, each olfactory sensory neuron chooses to express a single receptor in a stochastic process that includes substantial chromatin rearrangements. Here, we show that ants, which have the largest odorant receptor repertoires among insects, employ a different mechanism to regulate gene expression from tandem arrays. Using single-nucleus RNA sequencing, we found that ant olfactory sensory neurons choose different transcription start sites along an array but then produce mRNA from many downstream genes. This can result in transcripts from dozens of receptors being present in a single nucleus. Such rampant receptor co-expression at first seems difficult to reconcile with the narrow tuning of the ant olfactory system. However, RNA fluorescence in situ hybridization showed that only mRNA from the most upstream transcribed odorant receptor seems to reach the cytoplasm where it can be translated into protein, whereas mRNA from downstream receptors gets sequestered in the nucleus. This implies that, despite the extensive co-expression of odorant receptor genes, each olfactory sensory neuron ultimately only produces one or very few functional receptors. Evolution has thus found different molecular solutions in insects and mammals to the convergent challenge of selecting small subsets of receptors from large odorant receptor repertoires.

New species of Ancistrocerus (Vespidae, Eumeninae) from the Neotropics with a checklist and key to all species south of the Rio Grande.

A new species of potter wasp from South America, Ancistrocerus sursp. n., is described. A species key and checklist for all described Ancistrocerus that occur south of the Rio Grande are provided. New synonymy includes Odynerus bolivianus Brèthes = Ancistrocerus pilosus (de Saussure), while the subspecies bustamente discopictus Bequaert, lineativentris kamloopsensis Bequaert, lineativentris sinopis Bohart, tuberculocephalussutterianus (de Saussure), and pilosus ecuadorianus Bertoni, are all sunk under their respective nominotypical taxa.