Post-invasion selection acts on standing genetic variation despite a severe founding bottleneck.

Invasive populations often have lower genetic diversity relative to the native-range populations from which they derive.1,2 Despite this, many biological invaders succeed in their new environments, in part due to rapid adaptation.3,4,5,6 Therefore, the role of genetic bottlenecks in constraining the adaptation of invaders is debated.7,8,9,10 Here, we use whole-genome resequencing of samples from a 10-year time-series dataset, representing the natural invasion of the Asian honey bee (Apis cerana) in Australia, to investigate natural selection occurring in the aftermath of a founding event. We find that Australia's A. cerana population was founded by as few as one colony, whose arrival was followed by a period of rapid population expansion associated with an increase of rare variants.11 The bottleneck resulted in a steep loss of overall genetic diversity, yet we nevertheless detected loci with signatures of positive selection during the first years post-invasion. When we investigated the origin of alleles under selection, we found that selection acted primarily on the variation introduced by founders and not on the variants that arose post-invasion by mutation. In all, our data highlight that selection on standing genetic variation can occur in the early years post-invasion, even where founding bottlenecks are severe.

Thrice out of Asia and the adaptive radiation of the western honey bee.

The origin of the western honey bee Apis mellifera has been intensely debated. Addressing this knowledge gap is essential for understanding the evolution and genetics of one of the world's most important pollinators. By analyzing 251 genomes from 18 native subspecies, we found support for an Asian origin of honey bees with at least three expansions leading to African and European lineages. The adaptive radiation of honey bees involved selection on a few genomic "hotspots." We found 145 genes with independent signatures of selection across all bee lineages, and these genes were highly associated with worker traits. Our results indicate that a core set of genes associated with worker and colony traits facilitated the adaptive radiation of honey bees across their vast distribution.

Eusociality influences the strength of negative selection on insect genomes.

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.

A Single Gene Causes Thelytokous Parthenogenesis, the Defining Feature of the Cape Honeybee Apis mellifera capensis.

In honeybees, the ability of workers to produce daughters asexually, i.e., thelytokous parthenogenesis, is restricted to a single subspecies inhabiting the Cape region of South Africa, Apis mellifera capensis. Thelytoky has unleashed new selective pressures and the evolution of traits such as social parasitism, invasiveness, and social cancer. Thelytoky arises from an abnormal meiosis that results in the fusion of two maternal pronuclei, restoring diploidy in newly laid eggs. The genetic basis underlying thelytoky is disputed. To resolve this controversy, we generated a backcross between thelytokous A. m. capensis and non-thelytokous A. m. scutellata from the neighboring population and looked for evidence of genetic markers that co-segregated with thelytokous reproduction in 49 backcross females. We found that markers associated with the gene GB45239 on chromosome 11, including non-synonymous variants, showed consistent co-segregation with thelytoky, whereas no other region did so. Alleles associated with thelytoky were present in all A. m. capensis genomes examined but were absent from all other honeybees worldwide including A. m. scutellata. GB45239 is derived in A. m. capensis and has a putative role in chromosome segregation. It is expressed in ovaries and is downregulated in thelytokous bees, likely because of polymorphisms in the promoter region. Our study reveals how mutations affecting the sequence and/or expression of a single gene can change the reproductive mode of a population.

Recent advances in population and quantitative genomics of honey bees.

The increase in the availability of individual Apis mellifera genomes has resulted in significant progress toward understanding the evolution and adaptation of the honey bee. These efforts have identified new subspecies, evolutionary lineages, and a significant number of genes involved with adaptations and colony-level quantitative traits. Many studies have also developed genetic assays that are being used to monitor the movement and admixture of honey bee populations. These resources are valuable for conservation and breeding programs that seek to improve the economic value of colonies or preserve locally adapted populations and subspecies. This review provides a brief discussion on how population and quantitative genomic studies has improved our understanding of the honey bee.

Insects with similar social complexity show convergent patterns of adaptive molecular evolution.

Eusociality has independently evolved multiple times in the hymenoptera, but the patterns of adaptive molecular evolution underlying the evolution and elaboration of eusociality remain uncertain. Here, we performed a population genomics study of primitively eusocial Polistes (paper wasps), and compared their patterns of molecular evolution to two social bees; Bombus (bumblebees), and Apis (honey bees). This species triad allowed us to study molecular evolution across a gradient of social complexity (Polistes < Bombus < Apis) and compare species pairs that have similar (i.e. Polistes and Bombus) or different (i.e. Polistes and Apis) life histories, while controlling for phylogenetic distance. We found that regulatory genes have high levels of positive selection in Polistes; consistent with the prediction that adaptive changes in gene regulation are important during early stages of social evolution. Polistes and Bombus exhibit greater similarity in patterns of adaptive evolution including greater overlap of genes experiencing positive selection, and greater positive selection on queen-biased genes. Our findings suggest that either adaptive evolution of a few key genes underlie the evolution of simpler forms of eusociality, or that the initial stages of social evolution lead to selection on a few key traits orchestrated by orthologous genes and networks.