Dataset Information

Signatures of hybridization and speciation in genomic patterns of ancestry.

ABSTRACT: Genomes sampled from hybrid zones between nascent species provide important clues into the speciation process. With advances in genome sequencing and single nucleotide polymorphism (SNP) genotyping, it is now feasible to measure variation in gene flow with high genomic resolution. This progress motivates the development of conceptual and analytical frameworks for hybrid zones that complement well-established cline approaches. We extend the perspective that genomic distributions of ancestry are sensitive indicators of hybridization history. We use simulations to examine the behavior of the number of ancestry junctions-a simple summary of genomic patterns-in hybrid zones under increasingly realistic scenarios. Neutral simulations revealed that ancestry junction number is shaped by population structure, migration rate, and population size. Modeling multiple genetic architectures of hybrid dysfunction, with an emphasis on epistatic hybrid incompatibilities, showed that selection reduces junction number near loci that confer reproductive barriers. The magnitude of this signature was affected by the form of selection, dominance, and genomic location (autosome vs. sex chromosome) of incompatible loci. Our results suggest that researchers can identify loci involved in reproductive isolation by scanning hybrid genomes for local reductions in junction number. We outline necessary directions for future theory and method development to realize this goal.

SUBMITTER: Hvala JA

PROVIDER: S-EPMC6261709 | biostudies-literature | 2018 May

REPOSITORIES: biostudies-literature

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Signatures of hybridization and speciation in genomic patterns of ancestry.

Hvala John A JA Frayer Megan E ME Payseur Bret A BA

Evolution; international journal of organic evolution 20180528

Genomes sampled from hybrid zones between nascent species provide important clues into the speciation process. With advances in genome sequencing and single nucleotide polymorphism (SNP) genotyping, it is now feasible to measure variation in gene flow with high genomic resolution. This progress motivates the development of conceptual and analytical frameworks for hybrid zones that complement well-established cline approaches. We extend the perspective that genomic distributions of ancestry are s ...[more]

PMID: 29806154

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Project description:BackgroundSpeciation reversal: the erosion of species differentiation via an increase in introgressive hybridization due to the weakening of previously divergent selection regimes, is thought to be an important, yet poorly understood, driver of biodiversity loss. Our study system, the Alpine whitefish (Coregonus spp.) species complex is a classic example of a recent postglacial adaptive radiation: forming an array of endemic lake flocks, with the independent origination of similar ecotypes among flocks. However, many of the lakes of the Alpine radiation have been seriously impacted by anthropogenic nutrient enrichment, resulting in a collapse in neutral genetic and phenotypic differentiation within the most polluted lakes. Here we investigate the effects of eutrophication on the selective forces that have shaped this radiation, using population genomics. We studied eight sympatric species assemblages belonging to five independent parallel adaptive radiations, and one species pair in secondary contact. We used AFLP markers, and applied FST outlier (BayeScan, Dfdist) and logistic regression analyses (MatSAM), to identify candidate regions for disruptive selection in the genome and their associations with adaptive traits within each lake flock. The number of outlier and adaptive trait associated loci identified per lake were then regressed against two variables (historical phosphorus concentration and contemporary oxygen concentration) representing the strength of eutrophication.ResultsWhilst we identify disruptive selection candidate regions in all lake flocks, we find similar trends, across analysis methods, towards fewer disruptive selection candidate regions and fewer adaptive trait/candidate loci associations in the more polluted lakes.ConclusionsWeakened disruptive selection and a concomitant breakdown in reproductive isolating mechanisms in more polluted lakes has lead to increased gene flow between coexisting Alpine whitefish species. We hypothesize that the resulting higher rates of interspecific recombination reduce either the number or extent of genomic islands of divergence surrounding loci evolving under disruptive natural selection. This produces the negative trend seen in the number of selection candidate loci recovered during genome scans of whitefish species flocks, with increasing levels of anthropogenic eutrophication: as the likelihood decreases that AFLP restriction sites will fall within regions of heightened genomic divergence and therefore be classified as F(ST) outlier loci. This study explores for the first time the potential effects of human-mediated relaxation of disruptive selection on heterogeneous genomic divergence between coexisting species.

Project description:Hybridization can occur when two geographically isolated species are reproductively compatible and have come into sympatry due to range shifts. Yucca and yucca moths exhibit obligate pollination mutualism; yucca moths are responsible for the gene flow mediated by pollen among yucca populations. In the Baja California Peninsula, there are two yucca sister species, Y. capensis and Y. valida, that have coevolved with the same pollinator, Tegeticula baja. Both yucca species are endemic to the peninsula, and their current distributions are allopatric. Based on their morphological characteristics, it has been suggested that some plants growing in the southern part of the Magdalena flatland, a spatially disjunct part of Yucca valida's range, have hybrid origins. We conducted genomic and climatic analyses of the two yucca species as well as the putative hybrid populations. We genotyped 3,423 single nucleotide polymorphisms in 120 individuals sampled from 35 localities. We applied Bayesian tests and geographic cline analyses to the genomic data. Using climatic information from the occurrence sites, we projected species distribution models in different periods to assess changes in the distributional range, and we performed a statistical test to define the niche divergence between the paternal species and the putative hybrid populations. Structure analysis revealed mixed ancestry in the genome of hybrid populations, and the Bayesian models supported a scenario of post-divergence gene flow between the yucca species. Our species distribution models reveal that the geographical ranges of the parental species overlapped mainly during the Last Glacial Maximum, which could facilitate genetic admixture between those species. Finally, we found that most of the assessed environmental axes between the parents and hybrid populations are divergent, indicating that the climatic niche of the hybrid populations is shifting from that of the populations' progenitors. Our results show that the populations in the southern part of the Magdalena flatland are the result of combination of the genetic components of two species. Hybrid individuals with this novel genomic combination arose in a different habitat than their parental species, and they exhibit ecological divergence, which contributes to reproductive isolation through spatial and temporal barriers.

Dataset Information

Signatures of hybridization and speciation in genomic patterns of ancestry.

Publications

Signatures of hybridization and speciation in genomic patterns of ancestry.

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