Sociogenomics of Cooperation and Conflict during Colony Founding in the Fire Ant Solenopsis invicta

Abstract

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.

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

“…These queens were reared in the lab as previously described (Manfredini et al. 2013) to allow them to start new colonies. After worker emergence, incipient colonies were reared following standard conditions (Jouvenaz et al.…”

“…These samples were hybridized to 10 two‐color microarray chips containing more than 50K probes to unique transcripts (Roche NimbleGen, Inc., Madison WI) following a recently developed protocol (Manfredini et al. 2013, 2014). Expression data were analysed using a mixed‐model ANOVA as previously described (Manfredini et al.…”

The development of collective personality: the ontogenetic drivers of behavioral variation across groups

“…At least some of these changes in gene expression appear to precede changes in behavior and some have been demonstrated to have causal influences on individual behavioral tendencies (Page et al, 2012). The social environment, including colony maturation, can also have a profound influence on an individual's gene expression (honey bees Apis mellifera, Grozinger et al, 2003;Wang et al, 2008; fire ants Solenopsis invicta, Manfredini et al, 2013; paper wasps Polistes metricus, Toth et al, 2014), and it is the dynamic interplay between the genome and the social environment (a field referred to as "sociogenomics") that makes the development of colony-level behavior so complex and fascinating (Figure 3).…”

Characterization of Allele Diversity in a Microsatellite Locus: A Registry for <i>Solenopsis invicta</i>

“…This situation has been observed only in introduced populations, and the first report was in South America, a region of natural occurrence. However, there are other possibilities: 1) the pri-mers used were not efficient in detecting social condition, see [8]; 2) the colony likely has more than one queen ant; or 3) the only mtDNA lineage found among the worker ants investigated may be evidence of a young nest founded by pleometrosis, with the queen ants still cooperating [21].…”