Abstract
The fire ant Solenopsis invicta and its close relatives display an important social polymorphism involving differences in colony queen number. Colonies are headed by either a single reproductive queen (monogyne form) or multiple queens (polygyne form). This variation in social organization is associated with variation at the gene Gp-9, with monogyne colonies harboring only B-like allelic variants and polygyne colonies always containing b-like variants as well. We describe naturally occurring variation at Gp-9 in fire ants based on 185 full-length sequences, 136 of which were obtained from S. invicta collected over much of its native range. While there is little overall differentiation between most of the numerous alleles observed, a surprising amount is found in the coding regions of the gene, with such substitutions usually causing amino acid replacements. This elevated coding-region variation may result from a lack of negative selection acting to constrain amino acid replacements over much of the protein, different mutation rates or biases in coding and non-coding sequences, negative selection acting with greater strength on non-coding than coding regions, and/or positive selection acting on the protein. Formal selection analyses provide evidence that the latter force played an important role in the basal b-like lineages coincident with the emergence of polygyny. While our data set reveals considerable paraphyly and polyphyly of S. invicta sequences with respect to those of other fire ant species, the b-like alleles of the socially polymorphic species are monophyletic. An expanded analysis of colonies containing alleles of this clade confirmed the invariant link between their presence and expression of polygyny. Finally, our discovery of several unique alleles bearing various combinations of b-like and B-like codons allows us to conclude that no single b-like residue is completely predictive of polygyne behavior and, thus, potentially causally involved in its expression. Rather, all three typical b-like residues appear to be necessary.
Highlights
A main goal of evolutionary genetics is to document naturally occurring variation and to reconcile observed patterns with population history and demography, fitness consequences, and selection regimes at genes of interest [1,2]
Because variation in queen number represents a fundamental social polymorphism that is associated with a suit of important reproductive, demographic, and life history differences [14,15,16], variation at general protein-9 (Gp-9) is hypothesized to underlie the expression of major alternative adaptive syndromes in S. invicta
This latter result parallels the lack of evidence for recombination at Gp-9 reported by Krieger and Ross [11]
Summary
A main goal of evolutionary genetics is to document naturally occurring variation and to reconcile observed patterns with population history and demography, fitness consequences, and selection regimes at genes of interest [1,2]. Colonies with multiple reproductive queens (polygyne colonies) always have an alternate class of alleles, designated b-like alleles, represented along with B-like alleles among colony members [8,9,10,11] This pattern, coupled with similar genetic compositions of monogyne and polygyne populations at numerous other nuclear genes, has led to the hypothesis that the presence of b-like alleles in a colony’s workers is both necessary and sufficient to elicit polygyne social behavior [8,9,10,12,13]. Because variation in queen number represents a fundamental social polymorphism that is associated with a suit of important reproductive, demographic, and life history differences [14,15,16], variation at Gp-9 is hypothesized to underlie the expression of major alternative adaptive syndromes in S. invicta
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