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Cooperation among unrelated ant queens provides persistent growth and survival benefits during colony ontogeny.

ABSTRACT: The fitness consequences of cooperation can vary across an organism's lifespan. For non-kin groups, especially, social advantages must balance intrinsic costs of cooperating with non-relatives. In this study, we asked how challenging life history stages can promote stable, long-term alliances among unrelated ant queens. We reared single- and multi-queen colonies of the primary polygynous harvester ant, Pogonomyrmex californicus, from founding through the first ten months of colony growth, when groups face high mortality risks. We found that colonies founded by multiple, unrelated queens experienced significant survival and growth advantages that outlasted the colony founding period. Multi-queen colonies experienced lower mortality than single-queen colonies, and queens in groups experienced lower mortality than solitary queens. Further, multi-queen colonies produced workers at a faster rate than did single-queen colonies, even while experiencing lower per-queen worker production costs. Additionally, we characterized ontogenetic changes in the organization of labor, and observed increasing and decreasing task performance diversity by workers and queens, respectively, as colonies grew. This dynamic task allocation likely reflects a response to the changing role of queens as they are increasingly able to delegate risky and costly tasks to an expanding workforce. Faster worker production in multi-queen colonies may beneficially accelerate this behavioral transition from a vulnerable parent-offspring group to a stable, growing colony. These combined benefits of cooperation may facilitate the retention of multiple unrelated queens in mature colonies despite direct fitness costs, providing insight into the evolutionary drivers of stable associations between unrelated individuals.

SUBMITTER: Ostwald MM

PROVIDER: S-EPMC8050306 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:AbstractKey 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 statementUnderstanding 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.Supplementary informationThe online version contains supplementary material available at 10.1007/s00265-021-03105-1.

Project description:One of the fundamental questions in biology is how cooperative and altruistic behaviors evolved. The majority of studies seeking to identify the genes regulating these behaviors have been performed in systems where behavioral and physiological differences are relatively fixed, such as in the honey bee. During colony founding in the monogyne (one queen per colony) social form of the fire ant Solenopsis invicta, newly-mated queens may start new colonies either individually (haplometrosis) or in groups (pleometrosis). However, only one queen (the "winner") in pleometrotic associations survives and takes the lead of the young colony while the others (the "losers") are executed. Thus, colony founding in fire ants provides an excellent system in which to examine the genes underpinning cooperative behavior and how the social environment shapes the expression of these genes. We developed a new whole genome microarray platform for S. invicta to characterize the gene expression patterns associated with colony founding behavior. First, we compared haplometrotic queens, pleometrotic winners and pleometrotic losers. Second, we manipulated pleometrotic couples in order to switch or maintain the social ranks of the two cofoundresses. Haplometrotic and pleometrotic queens differed in the expression of genes involved in stress response, aging, immunity, reproduction and lipid biosynthesis. Smaller sets of genes were differentially expressed between winners and losers. In the second experiment, switching social rank had a much greater impact on gene expression patterns than the initial/final rank. Expression differences for several candidate genes involved in key biological processes were confirmed using qRT-PCR. Our findings indicate that, in S. invicta, social environment plays a major role in the determination of the patterns of gene expression, while the queen's physiological state is secondary. These results highlight the powerful influence of social environment on regulation of the genomic state, physiology and ultimately, social behavior of animals.

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Cooperation among unrelated ant queens provides persistent growth and survival benefits during colony ontogeny.

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