Strong hybrid male incompatibilities impede the spread of a selfish chromosome between populations of a fly

Abstract

Meiotically driving sex chromosomes manipulate gametogenesis to increase their transmission at a cost to the rest of the genome. The intragenomic conflicts they produce have major impacts on the ecology and evolution of their host species. However, their ecological dynamics remain poorly understood. Simple population genetic models predict meiotic drivers will rapidly reach fixation in populations and spread across landscapes. In contrast, natural populations commonly show spatial variation in the frequency of drivers, with drive present in clines or mosaics across species ranges. For example, Drosophila subobscura harbors a sex ratio distorting drive chromosome (SRs) at 15-25% frequency in North Africa, present at less than 2% frequency in adjacent southern Spain, and absent in other European populations. Here, we investigate the forces preventing the spread of the driver northward. We show that SRs has remained at a constant frequency in North Africa, and failed to spread in Spain. We find strong evidence that spread is impeded by genetic incompatibility between SRs and Spanish autosomal backgrounds. When we cross SRs from North Africa onto Spanish genetic backgrounds we observe strong incompatibilities specific to hybrids bearing SRs. The incompatibilities increase in severity in F2 male hybrids, leading to almost complete infertility. We find no evidence supporting an alternative hypothesis, that there is resistance to drive in Spanish populations. We conclude that the source of the stepped frequency variation is genetic incompatibility between the SRs chromosome and the genetic backgrounds of the adjacent population, preventing SRs spreading northward. The low frequency of SRs in South Spain is consistent with recurrent gene flow across the Strait of Gibraltar combined with selection against the SRs element through genetic incompatibility. This demonstrates that incompatibilities between drive chromosomes and naïve populations can prevent the spread of drive between populations, at a continental scale.

Keywords: Compatibility; Drosophila subobscura; X chromosome meiotic drive; segregation‐distortion; selfish genetic elements; suppression.

Figure 1

Map of driving and nondriving X chromosomes across Southern Europe and North Africa. Pie charts show the proportion of SRs (in black) and nondriving (white) X chromosomes. The numbers represent the years and sources of the collections (A—1968 [Jungen 1968], B—1974 [Prevosti 1974], C—1984 [Prevosti et al. 1984], D—2002 [Sole et al. 2002], E—2013–15 collections Table S2). Numbers next to the letters represent the number of X chromosomes sampled.

Figure 2

(A) The number of offspring produced by three different categories of X chromosome (SRs, nondriving Tunisian—Tu, nondriving Spanish—Sp) on different autosomal backgrounds (100% native autosomes or 50% foreign autosomes). Reduced fitness only occurs when SRs chromosomes occur in a hybrid background. Solid and dashed lined show the means and two SEM, respectively. (B) Mean number of offspring produced by SRs males with different genetic backgrounds, showing low fitness on hybrid backgrounds. Each point indicates the mean and 95% confidence intervals for a single isoline. Main lines show population means.

Figure 3

Scatterplot showing the number of offspring produced in seven days for males, which were introgressed into the Spanish population for two generations, carrying the Spanish X chromosome or the SRs chromosome. The X chromosome identity of males was confirmed using the SNP variation in the G6P locus (Supporting Information 1).

Figure 4

(A) Total offspring and (B) offspring sex ratios produced by hybrid Moroccan/Tunisian males carrying the Tunisian SRs (diamonds) and pure Tunisian control males carrying SRs (solid triangle). Points indicate the mean, whereas error bars indicate 95% confidence intervals.

Figure 5

Offspring sex ratio of SRs males on native and Spanish/Tunisian and United Kingdom/Tunisian hybrid backgrounds. Each point indicates the mean and 95% confidence intervals for a single isoline. Main lines show population means.