Sara Helms Cahan

Caste differentiation and division of labour are the hallmarks of insect societies¹ and at the root of their ecological success². Kin selection predicts that caste determination should result from environmentally induced differences in gene expression^3,4, a prediction largely supported by empirical data⁵. However, two exceptional cases of genetically determined caste differentiation have recently been found in harvester ants^6,7,8. Here we show that genetic caste determination evolved in these populations after complex hybridization events. We identified four distinct genetic lineages, each consisting of unique blends of the genomes of the parental species, presumably Pogonomyrmex barbatus and P. rugosus. Crosses between lineages H1 and H2 and between J1 and J2 give rise to workers, whereas queens develop from within-lineage matings. Although historical gene flow is evident, genetic exchange among lineages and between lineages and the parental species no longer occurs. This unusual system of caste determination seems to be evolutionarily stable.

Interspecific hybridization can often impose a substantial fitness cost due to reduced hybrid viability or fecundity. In social insects, however, such costs disproportionately impact reproductive offspring, whereas hybrids who become sterile workers can be functional, and even beneficial, colony members. Genomic imprinting of the paternal genome in reproductive, but not worker female offspring has been proposed as a mechanism to avoid genomic incompatibilities in hybrid queens in a hybrid zone between two fire ant species, Solenopsis geminata and S. xyloni. A study of allozyme variation demonstrated differences between the worker caste displaying a hybrid phenotype, and the winged queen caste displaying only the mother's phenotype. In this study, we investigate whether these differences are caused by genomic imprinting or genetic differences between castes by comparing variability of proteins to that of microsatellite markers. Workers and winged queens differed genetically at both classes of marker, indicating that allozyme differences were caused by underlying genetic differences between castes rather than differences in gene expression due to imprinting. Workers were F1 S. geminata x S. xyloni hybrids, whereas nearly all winged queens were of pure S. xyloni ancestry. Thus, S. xyloni within the hybrid zone appears to have evolved social hybridogenesis, in which the loss of worker potential in pure-species offspring necessitates hybridization for worker production, but prevents hybrids from being represented in the reproductive caste.

The process of reproductive caste determination in eusocial insect colonies is generally understood to be mediated by environmental, rather than genetic factors. We present data demonstrating unexpected genetic differences between reproductive castes in a variant of the rough harvester ant, Pogonomyrmex rugosus var. fuscatus. Across multiple loci, queens were consistently more homozygous than expected, while workers were more heterozygous. Adult colony queens were divided into two highly divergent genetic groups, indicating the presence of two cryptic species, rather than a single population. The observed genetic differences between castes reflect differential representation of heterospecific and conspecific patrilines in these offspring groups. All workers were hybrids; by contrast, winged queens were nearly all pure–species. The complete lack of pure–species workers indicates a loss of worker potential in pure–species female offspring. Hybrids appear to be bipotential, but do not normally develop into reproductives because they are displaced by pure–species females in the reproductive pool. Genetic differences between reproductive castes are expected to be rare in non–hybridizing populations, but within hybrid zones they may be evolutionarily stable and thus much more likely to occur.

Current research on the evolution of sociality seeks to integrate a wealth of species‐specific studies to draw more generalized conclusions. Developing a unified theory of social evolution has been a challenging process, hampered by the inherent complexity of social systems. By viewing a species’ social structure as the result of a series, or “trajectory”, of decisions individuals make about whether or not to disperse from their natal territory, whether to co‐breed or refrain from breeding, and whether or not to provide alloparental care, we can more easily evaluate whether selective factors influencing each social decision are similar across taxa. At the same time, the social trajectory framework highlights the interrelationships among different social decisions, both throughout the life of an individual and over evolutionary time. There are likely to be multiple unifying themes within sociality research; we hope that the simple framework outlined here will promote exchange between researchers across taxonomic disciplines to begin to identify common principles.