The evolution of eusociality is one of the major transitions in evolution, but the underlying genomic changes are unknown. We compared the genomes of 10 bee species that vary in social complexity, representing multiple independent transitions in social evolution, and report three major findings. First, many important genes show evidence of neutral evolution as a consequence of relaxed selection with increasing social complexity. Second, there is no single road map to eusociality; independent evolutionary transitions in sociality have independent genetic underpinnings. Third, though clearly independent in detail, these transitions do have similar general features, including an increase in constrained protein evolution accompanied by increases in the potential for gene regulation and decreases in diversity and abundance of transposable elements. Eusociality may arise through different mechanisms each time, but would likely always involve an increase in the complexity of gene networks.

The role of genetic factors in extinction is firmly established for diploid organisms, but haplodiploids have been considered immune to genetic load impacts because deleterious alleles are readily purged in haploid males. However, we show that singlelocus complementary sex determination ancestral to the haplodiploid Hymenoptera (ants, bees, and wasps) imposes a substantial genetic load through homozygosity at the sex locus that results in the production of inviable or sterile diploid males. Using stochastic modeling, we have discovered that diploid male production (DMP) can initiate a rapid and previously uncharacterized extinction vortex. The extinction rate in haplodiploid populations with DMP is an order of magnitude greater than in its absence under realistic but conservative demographic parameter values. Furthermore, DMP alone can elevate the base extinction risk in haplodiploids by over an order of magnitude higher than that caused by inbreeding depression in threatened diploids. Thus, contrary to previous expectations, haplodiploids are more, rather than less, prone to extinction for genetic reasons. Our findings necessitate a fundamental shift in approaches to the conservation and population biology of these ecologically and economically crucial insects.diploid male production ͉ haplodiploidy ͉ Hymenoptera ͉ pollinator decline ͉ conservation genetics H aplodiploid insects such as ants, bees, and wasps are crucial components of terrestrial ecosystems, and their conservation is essential for economic as well as ecological reasons (1-4). Despite the obvious differences that result from their sexdetermining mechanism, the conservation genetics of haplodiploids has received very little attention (5) and has been ignored in conservation efforts (6, 7). Inbreeding depression in diploid organisms significantly increases extinction risk (8-11), but faster purging of recessive deleterious mutations in haploid males is believed to render haplodiploids relatively immune to its effects (12-14), theoretically reducing their intrinsic extinction risk, compared with diploids. However, single-locus complementary sex determination (sl-CSD), ancestral in the Hymenoptera, introduces an unusual source of genetic load in small populations (15): the production of inviable or effectively sterile diploid males (DMs) from fertilized eggs homozygous at the sexdetermining locus, csd (16-19) (Fig. 1).Large haplodiploid populations can maintain many csd alleles (commonly 9-20 alleles; ref. 15) and thus have low levels of DM production (DMP). However, drift in small populations reduces csd allelic richness and increases DMP (15). Several studies have documented low levels of csd allelic richness (Ͻ5 alleles) in both natural and introduced populations (20-24). Because female hymenopterans fertilize their eggs to produce daughters only, the production of DMs effectively increases female mortality, thus reducing the potential for population growth (25) (Fig. 1). Further, DMP also reduces the effective breeding size of haplodiploids, espe...

Experiments linking neonicotinoids and declining bee health have been criticized for not simulating realistic exposure. Here we quantified the duration and magnitude of neonicotinoid exposure in Canada's corn-growing regions and used these data to design realistic experiments to investigate the effect of such insecticides on honey bees. Colonies near corn were naturally exposed to neonicotinoids for up to 4 months-the majority of the honey bee's active season. Realistic experiments showed that neonicotinoids increased worker mortality and were associated with declines in social immunity and increased queenlessness over time. We also discovered that the acute toxicity of neonicotinoids to honey bees doubles in the presence of a commonly encountered fungicide. Our work demonstrates that field-realistic exposure to neonicotinoids can reduce honey bee health in corn-growing regions.

Most theories used to explain the evolution of eusociality rest upon two key assumptions: mutations affecting the phenotype of sterile workers evolve by positive selection if the resulting traits benefit fertile kin, and that worker traits provide the primary mechanism allowing social insects to adapt to their environment. Despite the common view that positive selection drives phenotypic evolution of workers, we know very little about the prevalence of positive selection acting on the genomes of eusocial insects. We mapped the footprints of positive selection in Apis mellifera through analysis of 40 individual genomes, allowing us to identify thousands of genes and regulatory sequences with signatures of adaptive evolution over multiple timescales. We found Apoidea-and Apis-specific genes to be enriched for signatures of positive selection, indicating that novel genes play a disproportionately large role in adaptive evolution of eusocial insects. Worker-biased proteins have higher signatures of adaptive evolution relative to queen-biased proteins, supporting the view that worker traits are key to adaptation. We also found genes regulating worker division of labor to be enriched for signs of positive selection. Finally, genes associated with worker behavior based on analysis of brain gene expression were highly enriched for adaptive protein and cis-regulatory evolution. Our study highlights the significant contribution of worker phenotypes to adaptive evolution in social insects, and provides a wealth of knowledge on the loci that influence fitness in honey bees.natural selection | kin selection | social evolution | taxonomically restricted genes E usocial behavior evolved multiple times in insects and is characterized in part by extreme asymmetries in the reproductive potential of individuals (1). This asymmetry is most pronounced in advanced eusocial insects, with their fertile queen and sterile worker castes. Darwin first recognized that natural selection cannot directly optimize worker phenotypes because workers are usually sterile (2). Hamilton (3, 4) developed kinselection theory to describe the conditions that allow natural selection to indirectly optimize worker phenotypes if such phenotypes benefit their fertile kin. It is commonly believed that worker traits, such as sib-care, foraging, and colony defense, play important roles in allowing colonies to adapt to their environment (5-7). However, despite the central role of kin-selection and inclusive fitness theory in the field of Sociobiology (8, 9), we lack knowledge on the pattern and prevalence of positive selection acting on the genomes of eusocial insects.Population genomic studies provide unprecedented opportunities to detect signatures of selection on DNA sequences over different timescales (10). There are several tests of selection that can be applied to genome-wide datasets. The McDonald-Kreitman (MK) test is arguably the best method for detecting selection on protein coding sequences because of its robustness to changes in a species' demography,...

-The emerging threat of pollinator decline has motivated research on bee conservation biology in order to both understand the causes of declines and to develop appropriate conservation strategies. The application of genetics to the conservation of diploid animals has proven to be important for both overcoming genetic threats to population viability and for providing tools to guide conservation programs. However, the haplodiploid bees have several unusual genetic properties of relevance to their conservation, which warrant special attention. Here I review how haplodiploidy and complementary sex determination affect genetic parameters pertinent to the viability and future evolutionary potential of bee populations. I also review how genetic tools can improve the conservation management of bees. I find that bees are especially prone to extinction for genetic reasons, and that genetics can provide invaluable tools for managing bee populations to circumvent pollinator decline.haplodiploid / complementary sex determination / inbreeding depression / diploid males / extinction