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

Arthur Weyna,Jonathan Romiguier

doi:10.24072/pcjournal.3

Abstract

With one of the highest number of parasite, eusocial and pollinator species among all insect orders, Hymenoptera features a great diversity of specific lifestyles. At the population genetic level, such life-history strategies are expected to decrease effective population size and 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 or body size, but 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 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.

Highlights

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Because reproduction is typically monopolized by few long-lived reproductive individuals (Keller and Genoud, 1997), a decrease in long-term Ne and the efficiency of natural selection is often thought to be a general consequence of eusociality (Bromham and Leys, 2005; Romiguier et al, 2014b; Settepani et al, 2016)
Few studies have investigated how Ne 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)

Summary

Introduction

Peer Community Journal is a member of the Centre Mersenne for Open Scientific Publishing http:// www.centre-mersenne.org/. Recent studies with genome-wide datasets have detected associations between eusociality and decreases in Ne (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). We estimated mean genomic dN/dS for each species and compared these estimations between solitary and eusocial taxa, as well as between free and parasitic taxa. We correlated these to body size, life-history descriptor variables of parasitoids and geographical range descriptors. We found that, instead of large species, parasites or eusocial taxa, pollinating bees display by far the lowest long-term Ne among Hymenoptera

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Conclusion