Dataset Information

Dynamic changes in host-virus interactions associated with colony founding and social environment in fire ant queens (Solenopsis invicta).

ABSTRACT: The dynamics of host-parasite interactions can change dramatically over the course of a chronic infection as the internal (physiological) and external (environmental) conditions of the host change. When queens of social insects found a colony, they experience changes in both their physiological state (they develop their ovaries and begin laying eggs) and the social environment (they suddenly stop interacting with the other members of the mother colony), making this an excellent model system for examining how these factors interact with chronic infections. We investigated the dynamics of host-viral interactions in queens of Solenopsis invicta (fire ant) as they transition from mating to colony founding/brood rearing to the emergence of the first workers. We examined these dynamics in naturally infected queens in two different social environments, where queens either founded colonies as individuals or as pairs. We hypothesized that stress associated with colony founding plays an important role in the dynamics of host-parasite interactions. We also hypothesized that different viruses have different modalities of interaction with the host that can be quantified by physiological measures and genomic analysis of gene expression in the host. We found that the two most prevalent viruses, SINV-1 and SINV-2, are associated with different fitness costs that are mirrored by different patterns of gene expression in the host. In fact SINV-2, the virus that imposes the significant reduction of a queen's reproductive output is also associated with larger changes of global gene expression in the host. These results show the complexity of interactions between S. invicta and two viral parasites. Our findings also show that chronic infections by viral parasites in insects are dynamic processes that may pose different challenges in the host, laying the groundwork for interesting ecological and evolutionary considerations.

SUBMITTER: Manfredini F

PROVIDER: S-EPMC4716520 | biostudies-literature | 2016 Jan

REPOSITORIES: biostudies-literature

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Dynamic changes in host-virus interactions associated with colony founding and social environment in fire ant queens (Solenopsis invicta).

Manfredini Fabio F Shoemaker DeWayne D Grozinger Christina M CM

Ecology and evolution 20151229 1

The dynamics of host-parasite interactions can change dramatically over the course of a chronic infection as the internal (physiological) and external (environmental) conditions of the host change. When queens of social insects found a colony, they experience changes in both their physiological state (they develop their ovaries and begin laying eggs) and the social environment (they suddenly stop interacting with the other members of the mother colony), making this an excellent model system for ...[more]

PMID: 26811788

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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.

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.

Dataset Information

Dynamic changes in host-virus interactions associated with colony founding and social environment in fire ant queens (Solenopsis invicta).

Publications

Dynamic changes in host-virus interactions associated with colony founding and social environment in fire ant queens (Solenopsis invicta).

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