Population genomics of eusocial insects: the costs of a vertebrate‐like effective population size

Abstract

The evolution of reproductive division of labour and social life in social insects has lead to the emergence of several life-history traits and adaptations typical of larger organisms: social insect colonies can reach masses of several kilograms, they start reproducing only when they are several years old, and can live for decades. These features and the monopolization of reproduction by only one or few individuals in a colony should affect molecular evolution by reducing the effective population size. We tested this prediction by analysing genome-wide patterns of coding sequence polymorphism and divergence in eusocial vs. noneusocial insects based on newly generated RNA-seq data. We report very low amounts of genetic polymorphism and an elevated ratio of nonsynonymous to synonymous changes -a marker of the effective population size -in four distinct species of eusocial insects, which were more similar to vertebrates than to solitary insects regarding molecular evolutionary processes. Moreover, the ratio of nonsynonymous to synonymous substitutions was positively correlated with the level of social complexity across ant species. These results are fully consistent with the hypothesis of a reduced effective population size and an increased genetic load in eusocial insects, indicating that the evolution of social life has important consequences at both the genomic and population levels.

Patterns of cross-contamination in a multispecies population genomic project: detection, quantification, impact, and solutions

“…The relative bias was substantial – the median ratio of corrected to uncorrected π S was 0.90 when γ was 0.1, and 0.81 when γ was 0.2. The relative bias, however, was fairly constant across species, and much smaller that the between-species differences in π S , suggesting that our published comparative analyses of π S across species [17, 19, 21, 22] are robust to within-species contamination. We checked that the correlation reported by Romiguier et al [21] between π S and species life history traits were still valid after control for contamination.…”

A novel intracellular mutualistic bacterium in the invasive ant Cardiocondyla obscurior

“…In addition to reduced effective population sizes in host-associated bacteria compared with free-living relatives, small effective population size of C. obscurior (Schrader et al, 2014) and social insects in general (Romiguier et al, 2014) could lead to even faster genome degeneration. With a coding density of 70.76%, the genome is surprisingly loosely packed, compared with other endosymbionts with similar-length genomes (88% coding density on average) (McCutcheon and Moran, 2012).…”

Genomic signatures of evolutionary transitions from solitary to group living

“…Approximately two-thirds of these genes are under stronger directional selection in species with increasingly complex eusociality, but we also detected nonadaptive evolution. One-third of the rapidly evolving genes are under relaxed purifying selection in species with complex eusociality, possibly due to reduced effective population sizes (14). …”