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

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.

SUBMITTER: Baiz MD

PROVIDER: S-EPMC6888905 | biostudies-literature | 2019 Mar

REPOSITORIES: biostudies-literature

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

Baiz Marcella D MD Tucker Priscilla K PK Cortés-Ortiz Liliana L

Molecular ecology 20181224 5

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 ex ...[more]

PMID: 30582763

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Project description:BackgroundRing species, exemplified by salamanders of the Ensatina eschscholtzii complex, represent a special window into the speciation process because they allow the history of species formation to be traced back in time through the geographically differentiated forms connecting the two terminal forms of the ring. Of particular interest is the nature and extent of reproductive isolation between the geographically terminal forms, in this case E. e. eschscholtzii and E. e. klauberi. Previous studies have documented infrequent hybridization at the end of the ring. Here, we report the first fine-scale genetic analysis of a hybrid zone between the terminal forms in southern California using individual-based Bayesian analyses of multilocus genetic data to estimate levels and direction of hybridization and maximum-likelihood analysis of linkage disequilibrium and cline shape to make inferences about migration and selection in the hybrid zone.ResultsThe center of the hybrid zone has a high proportion of hybrids, about half of which were classified as F1s. Clines are narrow with respect to dispersal, and there are significant deviations from Hardy-Weinberg equilibrium as well as nonrandom associations (linkage disequilibria) between alleles characteristic of each parental type. There is cytonuclear discordance, both in terms of introgression and the geographic position of mitochondrial versus nuclear clines. Genetic disequilibrium is concentrated on the eschscholtzii side of the zone. Nearly all hybrids possess klauberi mtDNA, indicating that most hybrids are formed from female klauberi mating with male eschscholtzii or male hybrids (but not vice versa).ConclusionsOur results are consistent with a tension zone trapped at an ecotone, with gene combinations characteristic of klauberi showing up on the eschscholtzii side of the zone due to asymmetric hybridization. We suggest that the observed asymmetry is best explained by increased discriminatory power of eschscholtzii females, or asymmetric postzygotic isolation. The relatively high frequency of hybrids, particularly F1s, contrasts with other contacts between the terminal forms, and with other contacts between other divergent Ensatina lineages, highlighting the diverse outcomes of secondary contact within a single species complex.

Project description:BackgroundEvolution of reproductive isolation is an important process, generating biodiversity and driving speciation. To better understand this process, it is necessary to investigate factors underlying reproductive isolation through various approaches but also in various taxa. Previous studies, mainly focusing on diploid animals, supported the prevalent view that reproductive barriers evolve gradually as a by-product of genetic changes accumulated by natural selection by showing a positive relationship between the degree of reproductive isolation and genetic distance. Haplodiploid animals are expected to generate additional insight into speciation, but few studies investigated the prevalent view in haplodiploid animals. In this study, we investigate whether the relationship also holds in a haplodiploid spider mite, Amphitetranychus viennensis (Zacher).ResultsWe sampled seven populations of the mite in the Palaearctic region, measured their genetic distance (mtDNA) and carried out cross experiments with all combinations. We analyzed how lack of fertilization rate (as measure of prezygotic isolation) as well as hybrid inviability and hybrid sterility (as measures of postzygotic isolation) varies with genetic distance. We found that the degree of reproductive isolation varies among cross combinations, and that all three measures of reproductive isolation have a positive relationship with genetic distance. Based on the mtDNA marker, lack of fertilization rate, hybrid female inviability and hybrid female sterility were estimated to be nearly complete (99.0-99.9% barrier) at genetic distances of 0.475-0.657, 0.150-0.209 and 0.145-0.210, respectively. Besides, we found asymmetries in reproductive isolation.ConclusionsThe prevalent view on the evolution of reproductive barriers is supported in the haplodiploid spider mite we studied here. According to the estimated minimum genetic distance for total reproductive isolation in parent population crosses in this study and previous work, a genetic distance of 0.15-0.21 in mtDNA (COI) appears required for speciation in spider mites. Variations and asymmetries in the degree of reproductive isolation highlight the importance of reinforcement of prezygotic reproductive isolation through incompatibility and the importance of cytonuclear interactions for reproductive isolation in haplodiploid spider mites.

Project description:Background and aimsPolyploidy is an important contributor to sympatric speciation and assortative mating is a key mechanism driving cytotype interactions in contact zones. While strong reproductive barriers can mediate the coexistence of different cytotypes in sympatry, positive frequency-dependent mating disadvantage ultimately drives the transition to single-ploidy populations. However, comprehensive estimates of reproductive isolation among cytotypes and across multiple barriers are rare. We quantify the strength of isolation across multiple reproductive stages in a tetraploid-octoploid contact zone to understand the potential for coexistence.MethodsAssortative mating due to flowering asynchrony, pollinator behaviour, morphological overlap, self-fertilization and gametic competition between tetraploid and octoploid Gladiolus communis in a contact zone in the Western Iberian Peninsula were assessed in natural and experimental populations to quantify reproductive isolation (RI) between cytotypes.Key resultsTetraploids and octoploids have a high degree of overlap in flowering time and similar floral morphology, and are visited by generalist insects without cytotype foraging preferences, resulting in weak pre-pollination RI (from 0.00 to 0.21). In contrast, post-pollination isolation resulting from gametic selection was a strong barrier to inter-cytotype mating, with ploidy composition in stigmatic pollen loads determining the levels of RI (from 0.54 to 1.00). Between-cytotype cross-incompatibility was relatively high (RI from 0.54 to 0.63) as was isolation acquired through self-pollination (RI of 0.59 in tetraploids and 0.39 in octoploids).ConclusionsTotal RI was high for both tetraploids (from 0.90 to 1.00) and octoploids (from 0.78 to 0.98). Such high rates of assortative mating will enable cytotype coexistence in mixed-ploidy populations by weakening the impacts of minority cytotype exclusion. This study reveals the key role of gametic selection in cytotype siring success and highlights the importance of comprehensive estimates across multiple reproductive barriers to understand cytotype interactions at contact zones.

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

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

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