Eusociality influences the strength of negative selection on insect genomes

Abstract

While much of the focus of sociobiology concerns identifying genomic changes that influence social behaviour, we know little about the consequences of social behaviour on genome evolution. It has been hypothesized that social evolution can influence the strength of negative selection via two mechanisms. First, division of labour can influence the efficiency of negative selection in a caste-specific manner; indirect negative selection on worker traits is theoretically expected to be weaker than direct selection on queen traits. Second, increasing social complexity is expected to lead to relaxed negative selection because of its influence on effective population size. We tested these two hypotheses by estimating the strength of negative selection in honeybees, bumblebees, paper wasps, fire ants and six other insects that span the range of social complexity. We found no consistent evidence that negative selection was significantly stronger on queen-biased genes relative to worker-biased genes. However, we found strong evidence that increased social complexity reduced the efficiency of negative selection. Our study clearly illustrates how changes in behaviour can influence patterns of genome evolution by modulating the strength of natural selection.

No obvious transcriptome‐wide signature of indirect selection in termites

“…This convergent result with Imrit et al. (2020) suggests generality in our findings across several origins of eusociality.…”

“…Our results are more similar to Imrit et al. (2020) who found no consistent evidence from four social (hymenopteran) insect species that the strength of purifying selection was stronger on queen‐biased genes relative to worker‐biased genes. This convergent result with Imrit et al.…”

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

“…So far, few studies have investigated how N e varies among Hymenoptera, and all were restricted to the effect of eusociality alone (Berkelhamer, 1983;Bromham and Leys, 2005;Imrit et al, 2020;Owen, 1985;Reeve et al, 1985;Romiguier et al, 2014b). Only recent studies with genome-wide datasets have detected associations between eusociality and decreases in N e (Imrit et al, 2020;Romiguier et al, 2014b), but these studies are typically restricted to few taxa compared to studies that rejected any significant effect (Bromham and Leys, 2005). Disregarding the joint effect of other potential N e determinants (e.g., body-size, parasitism, pollen-feeding, haplo-diploidy) may bias results and explain the discrepancy among studies with low vs high number of species comparisons.…”

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

“…So far, few studies have investigated how Ne varies among Hymenoptera, and all were restricted to the effect of eusociality alone (Owen 1985;Berkelhamer 1983;Reeve et al 1985;Bromham and Leys 2005;Romiguier et al 2014;Imrit et al 2020). Only recent studies with genome-wide datasets have detected associations between eusociality and decreases in Ne (Romiguier et al 2014;Imrit et al 2020), but these studies are typically restricted to few taxa compared to studies that rejected any significant effect (Bromham and Leys 2005). Disregarding the joint effect of other potential Ne determinants (e.g., body-size, parasitism, pollen-feeding, haplo-diploidy) may bias results and explain the discrepancy among studies with low vs high number of species comparisons.…”