Asymmetric introgression between fishes in the Red River basin of Texas is associated with variation in water quality

Abstract

When ecologically divergent taxa encounter one another, hybrid zones can form when reproductive isolation is incomplete. The location of such hybrid zones can be influenced by environmental variables, and an ecological context can provide unique insights into the mechanisms by which species diverge and are maintained. Two ecologically differentiated species of small benthic fishes, the endemic and imperiled prairie chub, Macrhybopsis australis, and the shoal chub, Macrhybopsis hyostoma, are locally sympatric within the upper Red River Basin of Texas. We integrated population genomic data and environmental data to investigate species divergence and the maintenance of species boundaries in these two species. We found evidence of advanced-generation asymmetric hybridization and introgression, with shoal chub alleles introgressing more frequently into prairie chubs than the reciprocal. Using a Bayesian Genomic Cline framework, patterns of genomic introgression were revealed to be quite heterogeneous, yet shoal chub alleles were found to have likely selectively introgressed across species boundaries significantly more often than prairie chub alleles, potentially explaining some of the observed asymmetry in hybridization. These patterns were remarkably consistent across two sampled geographic regions of hybridization. Several environmental variables were found to significantly predict individual admixture, suggesting ecological isolation might maintain species boundaries.

Keywords: fish; genetic structure; hybridization; introgression; water quality variation.

Figure 1

Map of locales where shoal chubs and prairie chubs were collected on the Red River (RR), Pease River (PR), Wichita River (WR), and Brazos River (BR). The map inset at the top right depicts the broad sampling frame statewide. Shapes denoting the sampling locations represent purportedly shoal chubs (circles) and prairie chubs (triangles) based on meristic morphological assignments. Light gray shading represents the prairie chub distribution, dark gray shading represents the shoal chub distribution (Data provided by NatureServe, 2010). Site codes are defined in Table 1

Figure 2

PCA of genetic differentiation of all individuals from each collection locale. PC I explains approximately 39.76% of the genetic variation in the data, and PC II explains approximately 13.51% of the variation. Shapes and colors represent different collection locales. Black squares are individuals from the Brazos River, blue circles are individuals captured downstream of Lake Texoma on the Red River, red triangles are individuals from the Pease River, green diamonds are individuals captured upstream of Lake Texoma from the Red River, and purple triangles are individuals captured from the Wichita River

Figure 3

Entropy plots for k = 2 (a), 3 (b), and 4 (c) for all sampled sites oriented from most upstream to downstream (left to right) in the Red River basin, followed by the Brazos River. Site codes are defined in Table 1

Figure 4

Scatter plot showing the relationship between genome‐average ancestry (q1) and interpopulation ancestry (Q ₁₂). Symbols correspond to individuals from areas of the Red River basin (DS Texoma Red River = RR_259; Pease River = PR_287, PR_283, PR_6, and PR_104; US Texoma Red River = RR_35, RR_89, RR_81, RR_79, RR_70 and RR_283; Wichita River = WR_1919 and WR_6). Solid lines indicate the maximum possible interpopulation ancestry given global genetic ancestry

Figure 5

Median (± 95% CIs) of Bayesian genomic cline parameter α sorted by the lower 95% CI and by the upper 95% CI for hybrid individuals captured in the upstream (a, b) and downstream Red River (c, d). Upstream hybrids include individuals captured at RR_283, PR_287, PR_6, and WR_1919; downstream hybrids include individuals captured at RR_89, RR_81, RR_35, and RR_79. Number of loci considered exceptional due to their 95% CI not overlapping zero are given in the title of each respective plot