Unexpected patterns of segregation distortion at a selfish supergene in the fire ant Solenopsis invicta

Abstract

Background: The Sb supergene in the fire ant Solenopsis invicta determines the form of colony social organization, with colonies whose inhabitants bear the element containing multiple reproductive queens and colonies lacking it containing only a single queen. Several features of this supergene - including suppressed recombination, presence of deleterious mutations, association with a large centromere, and "green-beard" behavior - suggest that it may be a selfish genetic element that engages in transmission ratio distortion (TRD), defined as significant departures in progeny allele frequencies from Mendelian inheritance ratios. We tested this possibility by surveying segregation ratios in embryo progenies of 101 queens of the "polygyne" social form (3512 embryos) using three supergene-linked markers and twelve markers outside the supergene.

Results: Significant departures from Mendelian ratios were observed at the supergene loci in 3-5 times more progenies than expected in the absence of TRD and than found, on average, among non-supergene loci. Also, supergene loci displayed the greatest mean deviations from Mendelian ratios among all study loci, although these typically were modest. A surprising feature of the observed inter-progeny variation in TRD was that significant deviations involved not only excesses of supergene alleles but also similarly frequent excesses of the alternate alleles on the homologous chromosome. As expected given the common occurrence of such "drive reversal" in this system, alleles associated with the supergene gain no consistent transmission advantage over their alternate alleles at the population level. Finally, we observed low levels of recombination and incomplete gametic disequilibrium across the supergene, including between adjacent markers within a single inversion.

Conclusions: Our data confirm the prediction that the Sb supergene is a selfish genetic element capable of biasing its own transmission during reproduction, yet counterselection for suppressor loci evidently has produced an evolutionary stalemate in TRD between the variant homologous haplotypes on the "social chromosome". Evidence implicates prezygotic segregation distortion as responsible for the TRD we document, with "true" meiotic drive the most likely mechanism. Low levels of recombination and incomplete gametic disequilibrium across the supergene suggest that selection does not preserve a single uniform supergene haplotype responsible for inducing polygyny.

Keywords: Colony social organization; Meiotic drive; Segregation distortion; Selfish genetic element; Supergene; Transmission ratio distortion.

Fig. 1

Estimates of recombination frequencies (c) between pairs of marker loci. Triangles represent the mean values for jointly segregating embryo (egg) progenies, error bars represent the 95% confidence intervals (CIs), and circles represent the minimum and maximum values. White symbols represent locus pairs with c values significantly < 0.5

Fig. 2

Departures from Mendelian (1:1) segregation ratios in progeny embryos at 15 marker loci. a Observed proportions of progenies with significant non-Mendelian ratios (k > 0.5, one-tailed exact binomial tests, p < 0.05) at each locus. Blue-shaded bars represent the three supergene-associated loci; the hatched bar represents the proportion of departures based on simultaneous consideration of all three supergene-associated loci. The dotted line represents the mean proportion across the remaining twelve (non-supergene) loci (6.0%). Error bars for the observed departures represent the one-tailed lower 95% confidence limits derived from bootstrap/rarefaction analyses (Additional file 6: Text S2); bars that do not extend below 0.05 signify significant TRD for that locus. Inset―Observed proportions of progenies with k ≥ 0.65 (the threshold above which segregation ratios generally depart significantly from 1:1 with our sample sizes). Loci are arranged in the order: red_ant, C27, C536, i_114, Sol-42f, i_109, cassidy, Sol-49, i_129, i_120, sunrise, Bertha, Gp-9, C294, and i_126; supergene loci are represented by blue-shaded bars. b Boxplots depicting segregation proportions (k) for each segregating progeny at each locus; k values (unpolarized) represent the more common gamete allele in each such progeny in this graph. The boxes depict the interquartile ranges, with black horizontal lines representing the median and red lines the mean for each locus. Individual progenies with significant non-Mendelian ratios (binomial tests, p < 0.05) are indicated by the larger yellow circles. Supergene loci are represented by boxes shaded blue; loci in this graph are arranged from low to high mean k values

Fig. 3

Observed and simulated expected distributions of progeny segregation proportions (k) at three supergene-associated loci. The expected values were generated by a simulation model that takes into account specific sample sizes and assumes that departures from Mendelian segregation ratios arise by chance. The segregation proportions (polarized k) refer to the supergene-linked alleles C294⁹², Gp-9^b, and, for locus i_126, the specific allele on the supergene in each progeny (i_126²³⁰ in 60 of 85 [70.6%] segregating progenies). Hatching indicates proportions of progenies with observed k values that depart significantly from Mendelian ratios based on the binomial probabilities. Values on the x-axis denote bin maximum values of k

Fig. 4

Observed and simulated expected distributions of progenies with non-Mendelian segregation proportions of the Sb supergene. The distributions of expected numbers were generated by simulation models that simultaneously considered all three supergene-linked loci and accounted for specific sample sizes. The models assume that departures from Mendelian (1:1) segregation ratios arise solely by chance, with one model incorporating correlations between marker segregation ratios (black bars), and the other, more conservative model disregarding this non-independence (gray bars). Small arrows show the mean numbers of expected progenies from 1000 iterations of each model, whereas the large arrow shows the observed proportion of non-Mendelian progenies