Evolutionary genomics of socially polymorphic populations of Pogonomyrmex californicus.

BACKGROUND: Social insects vary considerably in their social organization both between and within species. In the California harvester ant, Pogonomyrmex californicus (Buckley 1867), colonies are commonly founded and headed by a single queen (haplometrosis, primary monogyny). However, in some populations in California (USA), unrelated queens cooperate not only during founding (pleometrosis) but also throughout the life of the colony (primary polygyny). The genetic architecture and evolutionary dynamics of this complex social niche polymorphism (haplometrosis vs pleometrosis) have remained unknown. RESULTS: We provide a first analysis of its genomic basis and evolutionary history using population genomics comparing individuals from a haplometrotic population to those from a pleometrotic population. We discovered a recently evolved (< 200 k years), 8-Mb non-recombining region segregating with the observed social niche polymorphism. This region shares several characteristics with supergenes underlying social polymorphisms in other socially polymorphic ant species. However, we also find remarkable differences from previously described social supergenes. Particularly, four additional genomic regions not in linkage with the supergene show signatures of a selective sweep in the pleometrotic population. Within these regions, we find for example genes crucial for epigenetic regulation via histone modification (chameau) and DNA methylation (Dnmt1). CONCLUSIONS: Altogether, our results suggest that social morph in this species is a polygenic trait involving a potential young supergene. Further studies targeting haplo- and pleometrotic individuals from a single population are however required to conclusively resolve whether these genetic differences underlie the alternative social phenotypes or have emerged through genetic drift.

The genomes of two key bumblebee species with primitive eusocial organization.

BACKGROUND: The shift from solitary to social behavior is one of the major evolutionary transitions. Primitively eusocial bumblebees are uniquely placed to illuminate the evolution of highly eusocial insect societies. Bumblebees are also invaluable natural and agricultural pollinators, and there is widespread concern over recent population declines in some species. High-quality genomic data will inform key aspects of bumblebee biology, including susceptibility to implicated population viability threats. RESULTS: We report the high quality draft genome sequences of Bombus terrestris and Bombus impatiens, two ecologically dominant bumblebees and widely utilized study species. Comparing these new genomes to those of the highly eusocial honeybee Apis mellifera and other Hymenoptera, we identify deeply conserved similarities, as well as novelties key to the biology of these organisms. Some honeybee genome features thought to underpin advanced eusociality are also present in bumblebees, indicating an earlier evolution in the bee lineage. Xenobiotic detoxification and immune genes are similarly depauperate in bumblebees and honeybees, and multiple categories of genes linked to social organization, including development and behavior, show high conservation. Key differences identified include a bias in bumblebee chemoreception towards gustation from olfaction, and striking differences in microRNAs, potentially responsible for gene regulation underlying social and other traits. CONCLUSIONS: These two bumblebee genomes provide a foundation for post-genomic research on these key pollinators and insect societies. Overall, gene repertoires suggest that the route to advanced eusociality in bees was mediated by many small changes in many genes and processes, and not by notable expansion or depauperation.

Social insect genomes exhibit dramatic evolution in gene composition and regulation while preserving regulatory features linked to sociality.

Genomes of eusocial insects code for dramatic examples of phenotypic plasticity and social organization. We compared the genomes of seven ants, the honeybee, and various solitary insects to examine whether eusocial lineages share distinct features of genomic organization. Each ant lineage contains ∼4000 novel genes, but only 64 of these genes are conserved among all seven ants. Many gene families have been expanded in ants, notably those involved in chemical communication (e.g., desaturases and odorant receptors). Alignment of the ant genomes revealed reduced purifying selection compared with Drosophila without significantly reduced synteny. Correspondingly, ant genomes exhibit dramatic divergence of noncoding regulatory elements; however, extant conserved regions are enriched for novel noncoding RNAs and transcription factor-binding sites. Comparison of orthologous gene promoters between eusocial and solitary species revealed significant regulatory evolution in both cis (e.g., Creb) and trans (e.g., fork head) for nearly 2000 genes, many of which exhibit phenotypic plasticity. Our results emphasize that genomic changes can occur remarkably fast in ants, because two recently diverged leaf-cutter ant species exhibit faster accumulation of species-specific genes and greater divergence in regulatory elements compared with other ants or Drosophila. Thus, while the "socio-genomes" of ants and the honeybee are broadly characterized by a pervasive pattern of divergence in gene composition and regulation, they preserve lineage-specific regulatory features linked to eusociality. We propose that changes in gene regulation played a key role in the origins of insect eusociality, whereas changes in gene composition were more relevant for lineage-specific eusocial adaptations.

The genomic impact of 100 million years of social evolution in seven ant species.

Ants (Hymenoptera, Formicidae) represent one of the most successful eusocial taxa in terms of both their geographic distribution and species number. The publication of seven ant genomes within the past year was a quantum leap for socio- and ant genomics. The diversity of social organization in ants makes them excellent model organisms to study the evolution of social systems. Comparing the ant genomes with those of the honeybee, a lineage that evolved eusociality independently from ants, and solitary insects suggests that there are significant differences in key aspects of genome organization between social and solitary insects, as well as among ant species. Altogether, these seven ant genomes open exciting new research avenues and opportunities for understanding the genetic basis and regulation of social species, and adaptive complex systems in general.

Ants (Formicidae): models for social complexity.

The family Formicidae (ants) is composed of more than 12,000 described species that vary greatly in size, morphology, behavior, life history, ecology, and social organization. Ants occur in most terrestrial habitats and are the dominant animals in many of them. They have been used as models to address fundamental questions in ecology, evolution, behavior, and development. The literature on ants is extensive, and the natural history of many species is known in detail. Phylogenetic relationships for the family, as well as within many subfamilies, are known, enabling comparative studies. Their ease of sampling and ecological variation makes them attractive for studying populations and questions relating to communities. Their sociality and variation in social organization have contributed greatly to an understanding of complex systems, division of labor, and chemical communication. Ants occur in colonies composed of tens to millions of individuals that vary greatly in morphology, physiology, and behavior; this variation has been used to address proximate and ultimate mechanisms generating phenotypic plasticity. Relatedness asymmetries within colonies have been fundamental to the formulation and empirical testing of kin and group selection theories. Genomic resources have been developed for some species, and a whole-genome sequence for several species is likely to follow in the near future; comparative genomics in ants should provide new insights into the evolution of complexity and sociogenomics. Future studies using ants should help establish a more comprehensive understanding of social life, from molecules to colonies.

Extreme queen-mating frequency and colony fission in African army ants.

Army ants have long been suspected to represent an independent origin of multiple queen-mating in the social Hymenoptera. Using microsatellite markers, we show that queens of the African army ant Dorylus (Anomma) molestus have the highest absolute (17.3) and effective (17.5) queen-mating frequencies reported so far for ants. This confirms that obligate multiple queen-mating in social insects is associated with large colony size and advanced social organization, but also raises several novel questions. First, these high estimates place army ants in the range of mating frequencies of honeybees, which have so far been regarded as odd exceptions within the social Hymenoptera. Army ants and honeybees are fundamentally different in morphology and life history, but are the only social insects known that combine obligate multiple mating with reproduction by colony fission and extremely male-biased sex ratios. This implies that the very high numbers of matings in both groups may be due partly to the relatively low costs of additional matings. Second, we were able to trace recent events of colony fission in four of the investigated colonies, where the genotypes of the two queens were only compatible with a mother-daughter relationship. A direct comparison of male production between colonies with offspring from one and two queens, respectively, suggested strongly that new queens do not produce a sexual brood until all workers of the old queen have died, which is consistent with kin selection theory.