Multiple forms of selection shape reproductive isolation in a primate hybrid zone - PubMed (original) (raw)

. 2019 Mar;28(5):1056-1069.

doi: 10.1111/mec.14966. Epub 2018 Dec 24.

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Multiple forms of selection shape reproductive isolation in a primate hybrid zone

Marcella D Baiz et al. Mol Ecol. 2019 Mar.

Abstract

Speciation occurs when populations diverge and become reproductively isolated from each other. Natural selection is commonly accepted to play a large role in this process, and it has been widely assumed that reproductive isolation often results as a by-product of divergence driven by adaptation in allopatry. When such populations come into secondary contact, reinforcement can act to strengthen reproductive isolation, but the frequency and importance of this process are still unknown. Here, we explored genomic signatures of selection in allopatry and sympatry for loci associated with reproductive isolation using a natural primate hybrid zone. By analysing reduced-representation sequencing data, we quantified admixture and population structure across a howler monkey hybrid zone and examined the relationship between locus-specific differentiation and introgression. We detected extensive admixture that was mostly limited to the narrow contact zone. Loci with reduced introgression into the heterospecific genomic background (the pattern expected for loci associated with reproductive isolation due to selection against hybrids) were significantly more differentiated between allopatric parental populations than loci with neutral and increased introgression, supporting the hypothesis that reproductive isolation is a by-product of divergence in allopatry. Further, loci with reduced introgression showed greater differentiation in sympatry than in allopatry, suggesting a role for reinforcement. Thus, our results reflect multiple forms of selection that have shaped reproductive isolation in this system. We conclude that reproductive isolation may have initially been driven by divergence in allopatry, but later reinforced by divergent selection in sympatry.

Keywords: Alouatta; admixture; genomic clines; introgression; population genomics; speciation.

© 2018 John Wiley & Sons Ltd.

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Figures

FIGURE 1

FIGURE 1

Sampling localities for individuals of the parental and hybrid populations. The range for Alouatta palliata is shown in yellow and the range for Alouatta pigra is in gray. Ver = Veracruz, Mexico, Tab = Tabasco, Mexico, Cam = Campeche, Mexico, DG = Dolores, Guatemala, QR = Quintana Roo, Mexico

FIGURE 2

FIGURE 2

Admixture proportions of sampled individuals. (a) fastStructure plot at K = 2 showing the geographical distribution of nonadmixed individuals and hybrids. Individuals are arranged from West (left) to East (right). Alouatta palliata ancestry is shown in yellow and Alouatta pigra ancestry is shown in gray. (b) Admixture proportion Q1 is closely correlated with bgc hybrid index for individuals in the hybrid zone (Tabasco, only representing individuals under the blue bar in the fastStructure plot)

FIGURE 3

FIGURE 3

Results of the principle component analysis. (a) PCA summarizing population structure among sampling sites. PC1 explains 55%, and PC2 explains 2.4% of the genetic variation among individuals. Open circles are nonadmixed individuals and triangles are hybrid individuals as determined by their admixture proportion (Q1) in fastStructure. (b) Admixture proportion Q1 is closely correlated with PC1. The gray line is a linear model fit to the data

FIGURE 4

FIGURE 4

Locus-specific point estimates for the genomic cline parameter β (amount of introgression) with β outliers in blue. β > 0 indicates reduced introgression, β < 0 indicates increased introgression. β = 0 indicates neutral introgression

FIGURE 5

FIGURE 5

Genetic differentiation between allopatric parental species. (a) Distribution of FST for all loci. (b) Boxplot showing FST for loci in each β category. Within each box, distribution medians are denoted by the vertical line and means are denoted with a black circle. Box height is equal to the 1st–3rd interquartile range. *p < 0.05; ***p < 0.001

FIGURE 6

FIGURE 6

The relationship between locus-specific differentiation in allopatry and sympatry for (a) loci with reduced introgression (β > 0) (_r_2 = 0.53, p < 2.2 × 10−16), (b) loci with neutral introgression (β = 0) (_r_2 = 0.76, p < 2.2 × 10−16), and (c) loci with increased introgression (β < 0) (_r_2 = 0.57, p < 2.2 × 10−16). In each case, the linear model fit to the data is represented by a solid black line with gray shading showing the 95% confidence interval of the slope, and the dashed red line indicates a 1:1 relationship

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