While it is well known that the genome can affect social behavior, recent models posit that social lifestyles can, in turn, influence genome evolution. Here, we perform the most phylogenetically comprehensive comparative analysis of 16 bee genomes to date: incorporating two published and four new carpenter bee genomes (Apidae: Xylocopinae) for a first-ever genomic comparison with a monophyletic clade containing solitary through advanced eusocial taxa. We find that eusocial lineages have undergone more gene family expansions, feature more signatures of positive selection, and have higher counts of taxonomically restricted genes than solitary and weakly social lineages. Transcriptomic data reveal that caste-affiliated genes are deeply-conserved; gene regulatory and functional elements are more closely tied to social phenotype than phylogenetic lineage; and regulatory complexity increases steadily with social complexity. Overall, our study provides robust empirical evidence that social evolution can act as a major and surprisingly consistent driver of macroevolutionary genomic change.

Facultatively social species exhibit behavioral plasticity in response to changes in ecological conditions and social environment, and thus provide a natural experiment to compare solitary and social behaviors in a single genome. Such species can therefore provide empirical insights into the evolution of eusociality. The small carpenter bees (genus Ceratina) and sweat bees (Halictidae) are of special interest because they exhibit rich behavioral plasticity. Species range from solitary to eusocial, and both groups benefit from detailed behavioral research and well-established phylogenies. As such, small carpenter and sweat bees are poised to further comparative sociogenomic studies which emphasize the necessity of a molecular phylogeny for understanding the evolution of molecular architecture underlying social phenotypes and organizational complexity. Here, we review behavioral, transcriptomic and genomic data in bees across the social spectrum, highlighting the importance of simple societies and facultatively social taxa to examine the genetic basis of cooperative traits and social evolution.

The evolutionary origins of advanced eusociality, one of the most complex forms of phenotypic plasticity in nature, have long been a focus within the field of sociobiology. Although eusocial insects are known to have evolved from solitary ancestors, sociogenomic research among incipiently social taxa has only recently provided empirical evidence supporting theories that modular regulation and deeply conserved genes may play important roles in both the evolutionary emergence and elaboration of insect sociality. There remains, however, a paucity of data to further test the biological reality of these and other evolutionary theories among taxa in the earliest stages of social evolution. Here, we present brain transcriptomic data from the incipiently social small carpenter bee, Ceratina calcarata , which captures patterns of cis -regulation and gene expression associated with female maturation, and underlying two well-defined behavioural states, foraging and guarding, concurrently demonstrated by mothers and daughters during early autumn. We find that an incipiently social nest environment may dramatically affect gene expression. We further reveal foraging and guarding behaviours to be putatively caste-antecedent states in C. calcarata , and offer strong empirical support for the operation of modular regulation, involving deeply conserved and differentially expressed genes in the expression of early social forms.

We use three allopatric populations of the stalk-eyed fly Teleopsis dalmanni from Southeast Asia to test two predictions made by the sex chromosome drive hypothesis for Haldane's rule. The first is that modifiers that suppress or enhance drive should evolve rapidly and independently in isolated populations. The second is that drive loci or modifiers should also cause sterility in hybrid males. We tested these predictions by assaying the fertility of 2066 males derived from backcross experiments involving two pairs of populations and found that the proportion of mated males that fail to produce any offspring ranged from 38 to 60% among crosses with some males producing strongly female-biased or male-biased sex ratios. After genotyping each male at 25-28 genetic markers we found quantitative trait loci (QTL) that jointly influence male sterility, sperm length, and biased progeny sex ratios in each pair of populations, but almost no shared QTL between population crosses. We also discovered that the extant X SR chromosome has no effect on sex ratio or sterility in these backcross males. Whether shared QTL are caused by linkage or pleiotropy requires additional study. Nevertheless, these results indicate the presence of a "cryptic" drive system that is currently masked by suppressing elements that are associated with sterility and sperm length within but not between populations and, therefore, must have evolved since the populations became isolated, i.e., in ,100,000 years. We discuss how genes that influence sperm length may contribute to hybrid sterility.A major challenge to those who study speciation is to determine the causes of early reproductive isolation between incipient species. One avenue for gaining insight into this issue is to investigate the causes of Haldane's rule, i.e., the observation that the heterogametic sex of hybrid offspring are more likely to be sterile or inviable than the homogametic sex (Haldane 1922). This phenomenon has been observed in a wide range of animal taxa and is believed to be a nearly ubiquitous phase of early speciation (Orr 1997). Given that alleles for sterility or inviability are expected to be selected against within populations, models for the evolution of hybrid dysfunction typically assume two or more genes, each of which is neutral or advantageous within a population but have deleterious joint effects when mismatched between populations. Two nonmutually exclusive explanations (Turelli 1998) have been proposed for why these epistatic interactions, known as Dobzhansky-Muller incompatibilities (Dobzhansky 1937;Muller 1940Muller , 1942Orr 1995), should arise more quickly in the heterogametic sex.The dominance hypothesis (Muller 1942;Orr 1993;Turelli and Orr 1995) assumes that if genes causing hybrid dysfunction are recessive, then the heterogametic sex will be affected more than the homogametic sex. This result is expected because the degenerate (or missing, in XO taxa) sex chromosome possessed by the heterogametic sex fails to mask recessive alleles present on it...

Bees fulfil a critical ecological role as pollinators, significantly contributing to the reproductive success of myriad angiosperm species. Although increasingly appreciated for their agricultural contributions, relatively little is yet known about the natural history of the vast majority of the more than 20 000 wild bee species worldwide. The small carpenter bee genus Ceratina occurs globally, and is represented in North America by its most recently diverged subgenera, Ceratinula and Zadontomerus. Recent genetic analysis of eastern Ceratina (Zadontomerus) supports the existence of five closely related, yet genetically distinct species living in sympatry. This phylogeographical study employs molecular barcoding of the most comprehensive specimen collection yet assembled to confirm the identities of these recently diverged eastern North American Ceratina (Zadontomerus) species. Delineation of extant population structure, evolutionary history and known range of this emerging model native pollinator are greatly improved by this study. We consider ecological and behavioural factors potentially contributing to the maintenance of genetic identity among these sympatric species.

The holobiont approach proposes that species are most fully understood within the context of their associated microbiomes, and that both host and microbial community are locked in a mutual circuit of co-evolutionary selection. Bees are an ideal group for this approach, as they comprise a critical group of pollinators that contribute to both ecological and agricultural health worldwide. Metagenomic analyses offer comprehensive insights into an organism’s microbiome, diet, and viral load, but remain largely unapplied to wild bees. Here, we present metagenomic data from three species of carpenter bees sampled from around the globe, representative of the first ever carpenter bee core microbiome. Machine learning, co-occurrence, and network analyses reveal that wild bee metagenomes are unique to host species. Further, we find that microbiomes are likely strongly affected by features of their local environment, and feature evidence of plant pathogens previously known only in honey bees. Performing the most comprehensive comparative analysis of bee microbiomes to date we discover that microbiome diversity is inversely proportional to host species social complexity. Our study helps to establish some of the first wild bee hologenomic data while offering powerful empirical insights into the biology and health of vital pollinators.

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