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

Abstract

Eusociality is a rare life history strategy that evolved repeatedly in Hymenoptera. At the population genetics level, inbreeding and low effective population size have been suggested as both evolutionary causes and consequences of social life. In this study, we tested these hypotheses by estimating the relative rate of non-synonymous substitution in 169 species to investigate the variation in natural selection efficiency and effective population size throughout the Hymenoptera tree of life. We show that relaxed selection is strongly associated with eusociality. This suggests that the division of reproductive labour decreases effective population size in ants, bees and wasps. Interestingly, we also report 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. We suggest that a particularly high inbreeding rate in bees might increase the benefits of kin selection, which would explain why most independent origins of eusociality in the tree of life occurred in this taxon. The particularly high load of deleterious mutations we report in the genome of these crucial ecosystem engineer species suggest new concerns about their ongoing population decline. RESULTS dN/dS distribution across the Hymenoptera phylogenyWe estimated dN/dS in 3241 gene alignments of 169 Hymenoptera species using the mapNH program (Romiguier et al. 2012, https://github.com/BioPP/testnh) from the testnh program suite (Dutheil and Boussau 2008;Guéguen and Duret 2018). Average genomic dN/dS values are displayed along the Hymenoptera tree on Figure 1. We used this tree obtained by Peters et al. (2017) and its topology thorough all analyses. The largest and smallest mean ratios were inferred for Eucera nigrescens (0.0745) and Macrocentrus marginator (0.0318). As expected for conserved coding regions, the distribution of genomic dN/dS ratios is close to 0 (overall average of 0.0424), indicative of the large prevalence of purifying selection. We observed above average dN/dS ratios in all 5 available eusocial clades: Formicidae (0.0463 ± 0.0019, 3 species), Polistinae/Vespinae wasps (0.0492 ± 0.0023, 3 species), Stenogastrinae (0.0447, 1 species only), the Apis/Bombus/Tetragonula clade (0.0511 ± 0.0057), and Halictidae (0.0613 ± 0.0039; 2 species). These last two clades of bees do not clearly stand out however, as most bees in the dataset (Antophila, species characterized by pollen feeding of larvae: Apidae, Megachilidae, Halictidae, Colettidae, Andrenidae, and Melittidae) show high dN/dS ratios (0.0522 ± 0.0073, 41 species) with no clear dependence on their social organization. Finally, only two purely solitary taxa displayed comparable dN/dS ratios: Siricoidea (0.0466 ± 0.0027, 3 species) and Cynipoidea (0.0447 ± 0.0059, 5 species). We further used simple linear modelling to try and relate variation in dN/dS ratios to life history traits. When needed, phylogenetic independent contrasts where used to account for phylogene...

Genomic signatures of recent convergent transitions to social life in spiders

“…Consistent with several previous studies in social spiders (33, 36–39) and social insects (26, 57, 58), we found that social branches tend to experience elevated genome-wide rates of molecular evolution (i.e. dN/dS) compared to nonsocial branches.…”

“…1A), which might be explained by lineage-specific differences in effective population size or other factors. Similarly, in a previous study in hymenopteran insects, social branches experienced elevated genome-wide dN/dS compared to nonsocial branches, but most variation existed between lineages, with bees --regardless social organization --having the highest dN/dS (58).…”

Multi-gene and lineage comparative assessment of the strength of selection in Hymenoptera

“…Using a previously published phylogenomic dataset containing 3256 genes and 169 hymenopteran species (Peters et al 2017), Weyna and Romiguier (2021) estimated mean genomic dN/dS ratios (nonsynonymous to synonymous substitution rates) for each species and compared these values between parasitic and nonparasitic species, eusocial and solitary species, and in relation to body size, parasitoid-specific traits and geographic range, thought to affect the effective population size and strength of selection. The use of a large number of species, as well as several distinct traits is a clear asset of this study.…”

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Relaxation of purifying selection suggests low effective population size in eusocial Hymenoptera and solitary pollinating bees (2021( ), bioRxiv, 2020 peer-reviewed and recommended by Peer Community in Evolutionary Biology.

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“…In this paper, Weyna and Romiguier (2021) set out to test if parasitism, body size, geographic range, and/or eusociality affect the strength of selection in Hymenoptera. Hymenoptera include the bees, wasps and ants and is an extraordinarily diverse order within the insects.…”