Social supergenes of superorganisms: do supergenes play important roles in social evolution?

We suggest that supergenes, groups of co-inherited loci, may be involved in a range of intriguing genetic and evolutionary phenomena in insect societies, and may play broad roles in the evolution of cooperation and conflict. Supergenes are central in the evolution of an array of traits including self-incompatibility, mimicry, and sex chromosomes. Recently, researchers identified a large supergene, described as a social chromosome, which controls social organization in the fire ant. This system was previously considered to be a remarkable example of a single gene affecting a complex social trait. We describe how selection may commonly favor reduced recombination and the formation of supergenes for social traits, and once formed, supergenes may strongly influence further evolutionary dynamics within and between lineages. The evolution of supergenes, and even wholly non-recombining genomes, may be particularly common in systems in which genetically distinct lineages can form mutually reinforcing socially parasitic relationships.

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.

Collecting live ant specimens (colony sampling).

Because of the great diversity of ants, it is difficult to give a single protocol for the collection of live specimens. Ant body size can be very small or extremely large; the ants can be hard or soft, sting or spray toxic chemicals, live in the open or in hard-to-reach places; and colony size can range from tens of individuals to millions. Thus, collection techniques must be tailored to each particular species. In particular, caution must always be taken when dealing with stinging species, and symptoms and basic first-aid measures, especially for the treatment of anaphylactic shock, should be reviewed before beginning fieldwork. Nonetheless, many species are collectable as whole colonies. This protocol reviews some basic techniques for collecting ground-nesting species and describes how to collect whole live colonies (with queens), which are necessary for long-term laboratory studies and addressing questions of social organization and ecology.