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

Abstract

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.

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

“…Natural selection is expected to be less efficient at removing superfluous genes from populations with small effective population sizes. Haplo-diploid sex determination and reproductive division of labor in eusocial Hymenoptera reduce effective population size relative to solitary and diploid Diptera (Crozier and Pamilo 1996;Gadau et al 2012). The lack of a significant codon usage bias in ant genomes compared with Drosophila further supports the idea of relatively reduced selection efficiency in eusocial Hymenoptera (Supplemental Fig.…”

“…Given the remarkable phenotypic diversity among eusocial insects, a key question is to what extent do derived and independent eusocial lineages harbor shared features of genomic organization that enable their eusocial lifestyles (Robinson et al 2005;Gadau et al 2012;Ferreira et al 2013). To address this question, we performed a comprehensive characterization of the genomic basis for eusociality, using eight eusocial insect genomes in addition to 22 available solitary insect genomes.…”

Genes and genomic processes underpinning the social lives of ants

“…These first seven ant genomes [2] led to a broad range of studies on these species (some examples below), but also paved the way for the sequencing of genomes and 'reference transcriptomes' of additional species. As of writing, genomes of 23 ant species and transcriptomes of 26 additional species have been published (Table 1).…”

“…Since their evolution from a solitary common ancestor $140 million years ago [2,3 ], the ants have radiated into >15 000 extant species. This ecologically dominant family exhibits an extraordinary diversity of social lifestyles, for example: obligatory fungus farming (leaf cutter ants), nomadic predatory lifestyles (army ants), slave-making and social parasitism [4].…”

“…While their behaviors, ecology, evolutionary contexts and morphologies have been extensively studied, it has only recently become possible to perform genome-scale analyses in ants [6], with the first seven ant genomes published in 2010 and 2011 [2]. Here, we review publications from the last few years on the genes and genomic processes underlying caste differentiation, the evolution of social organization, intraspecific variation in lifespan, symbiotic relationships, and chemical communication.…”