Cooperation by ant queens during colony-founding perpetuates alternative forms of social organization

Abstract

Key social traits, like queen number in eusocial insect colonies, have long been considered plastic, but the recent finding that colony social organization is under strict genetic control in multiple ant lineages challenges this view. This begs the question of which hardwired behavioral mechanism(s) generate alternative forms of social organization during colony development. We addressed this question in the Alpine silver ant, Formica selysi, a species with two social forms determined by a supergene. Queens that carry exclusively the M haplotype are produced by and live in monogyne (= single-queen) colonies, whereas queens that carry at least one copy of the P haplotype are produced by and live in polygyne (= multiple-queen) colonies. With extensive field samplings and laboratory experiments, we show that both types of queens successfully establish colonies independently, without being accompanied by workers, but that they do so in contrasting ways. Monogyne queens were generally intolerant of other queens and founded colonies solitarily, whereas polygyne queens were mutually attracted to each other and mainly founded colonies cooperatively. These associations persisted for months after worker emergence, suggesting that cooperative colony-founding leads to permanent multiple queening. Overall, our study shows that queens of each social form found colonies independently in the field but that P-carrying queens are more likely to cooperate, thereby contributing to perpetuate alternative forms of social organization. Significance statement Understanding the genetic and behavioral underpinnings of social organization is a major goal in evolutionary biology. Recent studies have shown that colony social organization is controlled by supergenes in multiple ant lineages. But the behavioral processes linking the genotype of a queen to the type of colony she will form remain largely unknown. Here, we show that in Alpine silver ants, alternative supergene genotypes are associated with different levels of social attraction and tolerance in young queens. These hardwired differences in social traits make queens carrying the P supergene haplotype more prone to cooperate and form durable associations during independent colony-founding. These findings help explain how genetic variants induce alternative forms of social organization during the ontogeny of a colony. They also illustrate how simple phenotypic differences at the individual level can result in large differences at higher levels of organization.

Effects of social organization and elevation on spatial genetic structure in a montane ant

“…These females of monogyne origin are larger and more successful at independent colony founding than females produced by polygyne colonies (De Gasperin et al, 2020; Reber et al, 2010; Rosset & Chapuisat, 2007). Some females of polygyne origin also disperse by flight and found colonies independently (Blacher et al, 2021; De Gasperin et al, 2020; Fontcuberta et al, 2021; Reber et al, 2010; Rosset & Chapuisat, 2006). Females from polygyne colonies tend to mate with slightly related males (Avril et al, 2019), which suggests that some of the polygyne females mate inside or close to their natal nest and forgo dispersal.…”

Iterative evolution of supergene-based social polymorphism in ants

“…‘M’, ‘FM’ and ‘P’ are used to denote the monogyne, functionally monogyne and polygyne social forms. Names of supergene haplotypes are italicized. Solenopsis invicta (Myrmicinae) Formica selysi (Formicinae) Leptothorax acervorum (Myrmicinae) Pogonomyrmex californicus (Myrmicinae) Cataglyphis niger (Formicinae)colony founding strategydependent (P) versus independent and alone (M) [37]independent and alone (M) versus dependent or independent and cooperative (P) [38,39]unknownindependent and alone (M) versus independent and cooperative (P) [40,41]likely dependent and independent (P and M) [42–44]mating behavioursmall-scale (P) versus large-scale (M) mating flights [37]mating flights (M) versus mating inside/around the nest and mating flights (P) [45,46]likely mating on the ground (FM & P) [47,48]mating flights (M and P) [41]mating on the ground (M and P; A. Hefetz 2021, personal communication)dispersalfar (M) versus local (P) [49]far (M) versus local (P) [38,50]unknownunknownunknownqueen morphologyM fatter [37]M larger [51,52]the same [47]same (J. Gadau 2021, personal communication)likely same (A. Hefetz 2021, personal communication)colony sizeP larger [27]P larger [38]same [47]P larger (J. Gadau 2021, personal communication)P larger [42–…”

“…These queens mate with M and P males, and produce M / P and P / P but not M / M daughters, for reasons discussed later. M / P and P / P queens are smaller than M / M queens, and can either perform mating flights, after which they tend to cooperate with other young queens to found polygynous colonies [39,50], or mate locally and return to an established polygyne colony [75]. As in S. invicta , polygyne colonies tend to contain more workers than monogyne colonies, and can likely be initiated via budding [38,76].…”

“…In the two species for which data are available on mating frequencies ( S. invicta and F. selysi [39]), there is non-random mating between queens and males of different genotypes [45,50,75,112], with important consequences for the evolutionary dynamics of the supergenes [45]. In US populations of S. invicta , all SB / SB queens and 80% of SB / Sb queens mate with SB males [70].…”

“…In this species, social organization is controlled by two haplotypes named P and M. In monogyne colonies all reproductive queens and workers are homozygous for the M haplotype. M/M queens are relatively large [38], perform mating flights [75] and found their own colonies independently [39], as in S. invicta. By contrast, polygyne colonies contain P/P and M/P reproductive queens.…”