Did the fire ant supergene evolve selfishly or socially?

Abstract

The genetic basis for animal social organization is poorly understood. Fire ants provide one of the rare cases where variation in social organization has been demonstrated to be under genetic control, which amazingly, segregates as a single Mendelian locus. A recent genetic, genomic, and cytological analysis revealed that this locus actually consists of over 600 genes locked together in a supergene that possesses many characteristics of sex chromosomes. The fire ant social supergene also behaves selfishly, and an interesting evolutionary question is whether the genes incorporated first into the social supergene were those for social adaptation, selfish genetic drive, or something else. In depth, functional molecular genetic analysis in fire ants and comparative genomics in other closely related socially polymorphic species will be required to resolve this question.

The fire ant social chromosome supergene variant Sb shows low diversity but high divergence from SB

“…Nevertheless, the fixation may instead have occurred in the source population before the invasion (Ascunce et al 2011), either due to a population bottleneck or a selective sweep. It is also possible that the fixation of the Sb supergene variant results from introgression of the chromosome from another Solenopsis species (Keller 1995;Krieger & Ross 2005;Huang & Wang 2014), similarly to the introgression of wing pattern mimicry alleles in butterflies (Smith & Kronforst 2013). Determining the timing of the fixation event would require studying the diversity of the Sb supergene variant in larger numbers of samples of different Solenopsis species in the native South American range (Huang & Wang 2014): a selective sweep or introgression event acting on South American populations would decrease genetic diversity in those populations as well as in North America, while a bottleneck during migration would have decreased genetic diversity only in North America.…”

“…; DeHeer ; Buechel et al . ; Huang & Wang ). Queens that will form their own single‐queen colony typically disperse over greater distances and can effectively colonize newly available habitats.…”

“…In this study, we focus on the evolution of a chromosome system responsible for two forms of social organization in the fire ant Solenopsis invicta (Wang et al 2013). Colonies have either exactly one queen or up to dozens of reproductive queens, with multiple physiological, morphological and behavioural traits differing between the two social forms (Ross & Keller 1995;DeHeer et al 1999;Keller & Ross 1999;Goodisman et al 2000;DeHeer 2002;Buechel et al 2014;Huang & Wang 2014). Queens that will form their own single-queen colony typically disperse over greater distances and can effectively colonize newly available habitats.…”

Fire ant social chromosomes: Differences in number, sequence and expression of odorant binding proteins

“…In contrast, multiple‐queen colonies can outcompete single‐queen colonies in saturated habitats and harsh environments, and can split by fission (Bourke and Heinze ; Ross and Keller ; Tschinkel ). Multiple additional traits differ between the two social forms, including in queen fecundity, colony size, worker size distribution, and worker aggressiveness (Ross and Keller ; DeHeer et al ; Keller and Ross ; Goodisman et al ; DeHeer ; Buechel et al ; Huang et al ).…”

Genomic architecture and evolutionary conflict drive allele-specific expression in the social supergene of the red fire ant

“…The first hypothesis is that evolutionary conflict drives differences in gene expression between social forms in a similar way to the generally accepted model of sex chromosome evolution (30). Assuming that high expression levels reflect a beneficial effect for the bearer (14), evolutionary conflict between social forms should lead to increased expression of genes favoring each of the social forms in each of the supergene variants (1,48). The alternative hypothesis is that the differences in expression between social forms are non-adaptive, instead reflecting genetic differentiation between SB and Sb at gene regulatory sites in the supergene region.…”