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Asymmetric Reproductive Barriers and Gene Flow Promote the Rise of a Stable Hybrid Zone in the Mediterranean High Mountain

ABSTRACT: Hybrid zones have the potential to shed light on evolutionary processes driving adaptation and speciation. Secondary contact hybrid zones are particularly powerful natural systems for studying the interaction between divergent genomes to understand the mode and rate at which reproductive isolation accumulates during speciation. We have studied a total of 720 plants belonging to five populations from two Erysimum (Brassicaceae) species presenting a contact zone in the Sierra Nevada mountains (SE Spain). The plants were phenotyped in 2007 and 2017, and most of them were genotyped the first year using 10 microsatellite markers. Plants coming from natural populations were grown in a common garden to evaluate the reproductive barriers between both species by means of controlled crosses. All the plants used for the field and greenhouse study were characterized by measuring traits related to plant size and flower size. We estimated the genetic molecular variances, the genetic differentiation, and the genetic structure by means of the F-statistic and Bayesian inference. We also estimated the amount of recent gene flow between populations. We found a narrow unimodal hybrid zone where the hybrid genotypes appear to have been maintained by significant levels of a unidirectional gene flow coming from parental populations and from weak reproductive isolation between them. Hybrid plants exhibited intermediate or vigorous phenotypes depending on the analyzed trait. The phenotypic differences between the hybrid and the parental plants were highly coherent between the field and controlled cross experiments and through time. The highly coherent results obtained by combining field, experimental, and genetic data demonstrate the existence of a stable and narrow unimodal hybrid zone between Erysimum mediohispanicum and Erysimum nevadense at the high elevation of the Sierra Nevada mountains.

SUBMITTER: Abdelaziz M

PROVIDER: S-EPMC8424041 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundOne key question in evolutionary biology deals with the mode and rate at which reproductive isolation accumulates during allopatric speciation. Little is known about secondary contacts of recently diverged anuran species. Here we conduct a multi-locus field study to investigate a contact zone between two lineages of green toads with an estimated divergence time of 2.7 My, and report results from preliminary experimental crosses.ResultsThe Sicilian endemic Bufo siculus and the Italian mainland-origin B. balearicus form a narrow hybrid zone east of Mt. Etna. Despite bidirectional mtDNA introgression over a ca. 40 km North-South cline, no F1 hybrids could be found, and nuclear genomes display almost no admixture. Populations from each side of the contact zone showed depressed genetic diversity and very strong differentiation (FST = 0.52). Preliminary experimental crosses point to a slightly reduced fitness in F1 hybrids, a strong hybrid breakdown in backcrossed offspring (F1 x parental, with very few reaching metamorphosis) and a complete and early mortality in F2 (F1 x F1).ConclusionGenetic patterns at the contact zone are molded by drift and selection. Local effective sizes are reduced by the geography and history of the contact zone, B. balearicus populations being at the front wave of a recent expansion (late Pleistocene). Selection against hybrids likely results from intrinsic genomic causes (disruption of coadapted sets of genes in backcrosses and F2-hybrids), possibly reinforced by local adaptation (the ranges of the two taxa roughly coincide with the borders of semiarid and arid climates). The absence of F1 in the field might be due to premating isolation mechanisms. Our results, show that these lineages have evolved almost complete reproductive isolation after some 2.7 My of divergence, contrasting sharply with evidence from laboratory experiments that some anuran species may still produce viable F1 offspring after > 20 My of divergence.

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.

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Asymmetric Reproductive Barriers and Gene Flow Promote the Rise of a Stable Hybrid Zone in the Mediterranean High Mountain

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