bioRxiv Science⌕ Search

bioRxiv · 10.1101/2020.04.14.038893

Relaxation of purifying selection suggests low effective population size in eusocial Hymenoptera and pollinating bees

Abstract

With one of the highest number of parasitic, eusocial and pollinator species among all insect orders, Hymenoptera features a great diversity of lifestyles. At the population genetic level, such life-history strategies are expected to decrease effective population size and the efficiency of purifying selection. In this study, we tested this hypothesis by estimating the relative rate of non-synonymous substitution in 169 species to investigate the variation in natural selection efficiency throughout the hymenopteran tree of life. We found no effect of parasitism, but we show that relaxed selection is associated with eusociality, suggesting that the division of reproductive labour decreases effective population size in ants, bees and wasps. Unexpectedly, the effect of eusociality is marginal compared to a striking and widespread relaxation of selection in both social and non social bees, which indicates that these keystone pollinator species generally feature low effective population sizes. This widespread pattern suggests specific constraints in pollinating bees potentially linked to limited resource availability and high parental investment. The particularly high load of deleterious mutations we report in the genome of these crucial ecosystem engineer species also raises new concerns about their ongoing population decline. This article has been peer-reviewed and recommended by Peer Community in Evolutionary Biology https://doi.org/10.24072/pci.evolbiol.100120

Source connections

Explore related subjects

Keep this discovery

Explore connections, maps & timelines

BibTeXRIS

Romiguier, J., Weyna, A.. 2020-04-15. Relaxation of purifying selection suggests low effective population size in eusocial Hymenoptera and pollinating bees. https://doi.org/10.1101/2020.04.14.038893

Cite the original work for its findings. Save a collection to share your selection of sources.

KEEP EXPLORING

Related preprints

Global homeostatic forces shape the composition of a hyperdiverse tropical insect fauna

Despite comprising the bulk of terrestrial biodiversity, we know surprisingly little about insect faunas, particularly in the tropics. Here, we characterize the insect fauna of Madagascar, a global biodiversity hotspot, based on extensive DNA metabarcoding of Malaise trap and leaf litter samples. We estimate that the fauna comprises at least 250,000 species, only 5% of which are currently recorded. The ecological and taxonomic composition is surprisingly similar to that of temperate forests. We show that this is likely caused by global homeostatic forces shaping net diversification rates after colonization of Madagascar rather than by the composition of colonizing lineages. Features differing from temperate forests include the dearth of parasitoids and richness of beetles. Understanding the forces shaping these patterns is key in sustainable management of tropical insect faunas.

evolutionary biology↗

Do divergent mitochondrial backgrounds alter the fate of nuclear alleles during hybridization and admixture?

Hybridization brings together genetic variation from different populations or species into admixed genomes. As selection sorts this variation, the fate of each allele is determined by its fitness effect in the new hybrid genomic background. Because mitochondrial genes coevolve with the nuclear genome, they may be especially sensitive to foreign nuclear backgrounds, making them potential "hot-spots" for hybrid incompatibilities. Here, we test whether selection against mitonuclear incompatibilities drives repeatable hybridization outcomes. Specifically, we experimentally evolved three sets of five populations of hybrid Drosophila melanogaster, each carrying the same nuclear chromosomes but paired with one of three increasingly divergent mitochondrial DNA backgrounds. We hypothesized that accumulated incompatibilities would result in different patterns of nuclear admixture among mitochondrial backgrounds. To test this, we tracked nuclear allele frequencies in all 15 populations by whole-genome sequencing at intermediate time points. After 25 generations, we observed that rapid genomic evolution produced a strikingly parallel mosaic of both nuclear ancestries, independent of mitochondrial background. Contrary to our hypothesis, we found no evidence that mitochondrial background1 shaped nuclear admixture, even for interspecific combinations. These results suggest that in species with large effective population sizes, efficient purifying selection limits the accumulation of mitonuclear incompatibilities, allowing selection on nuclear alleles to promote repeatable ancestry sorting immediately following hybridization.

evolutionary biology↗

Body size cascades from Neodiprion sawfly hosts to Perilampid parasitoids: An investigation of sequential divergence

Ecological speciation drives diversity in plant-eating insect systems, but it may also generate parallel specialization in parasitoid associates in a cascading effect of "sequential divergence." However, sequential divergence has never been successfully identified in parasitoids of externally feeding insects. To address this gap, we consider the Pinus-Neodiprion-Perilampus neodiprioni system, where plant-associated, externally feeding Neodiprion demonstrate ecological divergence, as supported by body size as a magic trait in sympatric species. It seems possible that this body size differentiation may cascade to Neodiprion's parasitoids via sequential divergence. Therefore, we asked, "Does P. neodiprioni exhibit host-specific divergence in body size that parallels patterns in Neodiprion hosts?" Further, "Does P. neodiprioni exhibit host-related variation in the abdominal region or sexually dimorphic features, supporting reproductive barriers?" Using by-catch samples, we measured body size of P. neodiprioni, reared from Neodiprion lecontei and Neodiprion pinetum hosts. We analyzed body size variation as predicted by host species, parasitoid sex, host sex, host cocoon size, latitude, and their interactions. In addition, we used mixed models to analyze the effects of parasitoid sex and Neodiprion host on three size-based facial features. We found that P. neodiprioni demonstrates host-associated body size variation that mirrors size differences in their Neodiprion hosts. In addition, host-associated size variation occurs in the abdominal region and two sexually dimorphic characters of P. neodiprioni, supporting possible reproductive isolation. Together, these patterns suggest that host magic traits may drive not only within-species ecological divergence, but they can facilitate parasitoids' subsequent morphological differentiation and possible sequential divergence.

evolutionary biology↗