Population genomics reveals a possible history of backcrossing and recombination in the gynogenetic fish Poecilia formosa

Abstract

Unisexual sperm-dependent vertebrates are of hybrid origins, rare, and predicted to be short-lived as a result of several challenges arising from their mode of reproduction. In particular, because of a lack of recombination, clonal species are predicted to have a low potential to respond to natural selection. However, many unisexual sperm-dependent species persist, and assessing the genetic diversity present in these species is fundamental to understanding how they avoid extinction. We used population genomic methods to assess genotypic variation within the unisexual fish Poecilia formosa. Measures of admixture and population differentiation, as well as clustering analyses, indicate that the genomes of individuals of P. formosa are admixed and intermediate between Poecilia latipinna and Poecilia mexicana, consistent with the hypothesis of their hybrid origins. Bayesian genomic cline analyses indicate that about 12% of sampled loci exhibit patterns consistent with inheritance from only one parent. The estimation of observed heterozygosity clearly suggests that P. formosa is not comprised of direct descendants of a single nonrecombining asexual F1 hybrid individual. Additionally, the estimation of observed heterozygosity provides support for the hypothesis that the history of this unisexual species has included backcrossing with the parent species before the onset of gynogenesis. We also document high levels of variation among asexual individuals, which is attributable to recombination (historical or ongoing) and the accumulation of mutations. The high genetic variation suggests that this unisexual vertebrate has more potential to respond to natural selection than if they were frozen F1 hybrids.

Fig. 1.

Sampled populations (A) and PCA plots for the 192 individuals based on the genotype probabilities at each locus (B–D). Dark blue, north P. latipinna; blue, central P. latipinna; light blue, south P. latipinna; orange, north P. formosa sympatric with P. latipinna; red, south P. formosa sympatric with P. mexicana; light green, north P. mexicana; green, central P. mexicana; dark green, south P. mexicana.

Fig. 2.

Results from STRUCTURE clustering analyses. Admixture proportion for K = 2 (A) and mean assignment probabilities to cluster 1 ±95% credible intervals for K = 2 (B). Admixture proportions for K = 4 (C) and mean assignment probability ±95% credible intervals for K = 4 for cluster individuals were assigned to D. K = 2 and K = 4 were chosen as the appropriate number of groups after examination of the log of the marginal likelihood and the ad hoc delta(K) statistic (41) for each K (Fig. S6).

Fig. 3.

Posterior probability of estimates of hybrid indices and cline parameter α for P. formosa. The assigned putative parent populations were P. mexicana found in the northern part of its range and P. latipinna found in the southern part of its range. A depicts the posterior probability distribution of the hybrid index estimates (±95% credible intervals) for the 41 P. formosa used in this study. The vertical dotted line in A divides P. formosa sympatric with P. latipinna (Left) from P. formosa sympatric with P. mexicana (Right). Each black line in B represents the 95% credible interval for the estimate of the cline parameter α for each of the 26,313 SNPs, for all 41 P. formosa. C shows the correlation between the alpha estimates at each locus in the populations of P. formosa in the south vs. populations in the north.