Iterative evolution of supergene-based social polymorphism in ants

Abstract

Species commonly exhibit alternative morphs, with individual fate being determined during development by either genetic factors, environmental cues or a combination thereof. Ants offer an interesting case study because many species are polymorphic in their social structure. Some colonies contain one queen while others contain many queens. This variation in queen number is generally associated with a suite of phenotypic and life-history traits, including mode of colony founding, queen lifespan, queen–worker dimorphism and colony size. The basis of this social polymorphism has been studied in five ant lineages, and remarkably social morph seems to be determined by a supergene in all cases. These ‘social supergenes’ tend to be large, having formed through serial inversions, and to comprise hundreds of linked genes. They have persisted over long evolutionary timescales, in multiple lineages following speciation events, and have spread between closely related species via introgression. Their evolutionary dynamics are unusually complex, combining recessive lethality, spatially variable selection, selfish genetic elements and non-random mating. Here, we synthesize the five cases of supergene-based social polymorphism in ants, highlighting interesting commonalities, idiosyncrasies and implications for the evolution of polymorphisms in general. This article is part of the theme issue ‘Genomic architecture of supergenes: causes and evolutionary consequences’.

Unbalanced selection: the challenge of maintaining a social polymorphism when a supergene is selfish

“…Here, we present a model examining the conditions for the long-term persistence of a polymorphism in a supergene controlling alternative forms of social organization in ants (reviewed in [ 14 ]), in which one haplotype is a transmission ratio distorter. The model is designed to fit the properties of the Alpine silver ant, Formica selysi .…”

Mutation accumulation opposes polymorphism: supergenes and the curious case of balanced lethals

“…For example, Formica ants show an elaborate social polymorphism, where colonies can be headed by either one or multiple queens (monogyne or polygyne colonies), with social morphs further differing in many other life-history traits (related to how colonies are founded, the longevity of queens, etc.) [ 50 , 51 ]. Monogyne colonies (homokaryotype queens) are better at colonizing new habitat patches (i.e.…”

Cryptic recessive lethality of a supergene controlling social organization in ants

“…However, the lifetime fitness of each of the three supergene genotypes is difficult to estimate, because the ant social forms differ in many life-history traits, including dispersal and colony founding (Fontcuberta et al, 2021;Rosset & Chapuisat, 2007;Tafreshi et al, 2022). Moreover, colony-level selection and various forms of density-and frequency-dependent selection can help stabilize the polymorphism (Zahnd et al, 2021) Chapuisat, 2023;Kay et al, 2022). Our results show another important and striking similarity between these social supergenes: deleterious effects of the derived, polygyny-inducing haplotype.…”