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Speciation and subsequent secondary contact in two edaphic endemic primroses driven by Pleistocene climatic oscillation.

ABSTRACT: Climatic perturbation during the Pleistocene era has played a major role in plant evolutionary history by altering species distribution range. However, the relative roles of climatic and geographic factors in the distribution dynamics remain poorly understood; in particular, the edaphic endemics. In this paper, we examine the evolutionary history of two ultramafic primroses, Primula hidakana and Primula takedana. These species are ecologically and morphologically distinct with disjunct distributions on Hokkaido Island, Japan. Primula hidakana is found on various rocks in southern Hokkaido and P. takedana in serpentine areas in northern Hokkaido. We performed population genetics analyses on nuclear and chloroplast data sets and tested alternative phylogenetic models of divergence using approximate Bayesian computation (ABC) analyses. Nuclear microsatellite loci clearly distinguished the two sister taxa. In contrast, chloroplast sequence variations were shared between P. takedana and P. hidakana. ABC analyses based on nuclear data supported a secondary contact scenario involving asymmetrical gene flow from P. hidakana to P. takedana. Paleodistribution modeling also supported the divergence model, and predicted their latitudinal range shifts leading to past secondary contact. Our findings highlight the importance of the distribution dynamics during the Pleistocene climatic oscillations in the evolution of serpentine plants, and demonstrate that tight species cohesion between serpentine and nonserpentine sister taxa has been maintained despite past interspecific gene flow across soil boundaries.

SUBMITTER: Yamamoto M

PROVIDER: S-EPMC6906382 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Background and aimsRecent biogeographic studies have illustrated that Quaternary climatic changes and historical orogenies have driven the development of high levels of biodiversity. In this context, phylogenetic niche conservatism may play a role as a major precursor of allopatric speciation. However, the effects of niche evolution on the diversification patterns of plant species under rapid habitat changes are still unknown. Here, Primula section Reinii, one of the few primroses endemic to the Japanese Archipelago, was investigated. This study aimed to clarify the phylogenetic position and relationships of section Reinii, interpret the biogeographic and diversification patterns of this group and gain a better understanding of the role of climatic niche evolution in the Japanese endemic primroses.MethodsDated phylogeny for Primula section Reinii is presented based on the sequences of six chloroplast genes and one nuclear gene. Biogeographic history was reconstructed using statistical dispersal-vicariance analysis. Macro-evolutionary modelling of the climatic niche was combined with biogeographic inferences.Key resultsSection Reinii was shown to be monophyletic based on chloroplast and nuclear sequences. Fossil-calibrated dating analysis estimated that this section diverged from its sister taxon, sect. Cortusoides, around 1.82 million years ago, and intraspecific diversification occurred within the last million years. This time frame was characterized by Quaternary climatic oscillations and uplift of high mountains in Japan. Biogeographic inference suggested that this section originated at the northern end of the Japanese Archipelago and then dispersed southward to other islands. Models of climatic niche evolution indicated that the closely related species P. reinii and P. tosanensis have contrasting niche optima and rates of niche evolution.ConclusionOur results highlight that spatiotemporal heterogeneity in the Japanese islands may play a significant role in the biogeographic history of Japanese endemic primroses. Contrasting evolutionary processes found in closely related species illustrate the effects of climatic niche evolution on species' diversification patterns.

Project description:BackgroundHaldane's Rule, the tendency for the heterogametic sex to show reduced fertility in hybrid crosses, can obscure the signal of gene flow in mtDNA between species where females are heterogametic. Therefore, it is important when studying speciation and species limits in female-heterogametic species like birds to assess the signature of gene flow in the nuclear genome as well. We studied introgression of microsatellites and mtDNA across a secondary contact zone between coastal and interior lineages of Western Scrub-Jays (Aphelocoma californica) to test for a signature of Haldane's Rule: a narrower cline of introgression in mtDNA compared to nuclear markers.ResultsOur initial phylogeographic analysis revealed that there is only one major area of contact between coastal and interior lineages and identified five genetic clusters with strong spatial structuring: Pacific Slope, Interior US, Edwards Plateau (Texas), Northern Mexico, and Southern Mexico. Consistent with predictions from Haldane's Rule, mtDNA showed a narrower cline than nuclear markers across a transect through the hybrid zone. This result is not being driven by female-biased dispersal because neutral diffusion analysis, which included estimates of sex-specific dispersal rates, also showed less diffusion of mtDNA. Lineage-specific plumage traits were associated with nuclear genetic profiles for individuals in the hybrid zone, indicating that these differences are under genetic control.ConclusionsThis study adds to a growing list of studies that support predictions of Haldane's Rule using cline analysis of multiple loci of differing inheritance modes, although alternate hypotheses like selection on different mtDNA types cannot be ruled out. That Haldane's Rule appears to be operating in this system suggests a measure of reproductive isolation between the Pacific Slope and interior lineages. Based on a variety of evidence from the phenotype, ecology, and genetics, we recommend elevating three lineages to species level: A. californica (Pacific Slope); A. woodhouseii (Interior US plus Edwards Plateau plus Northern Mexico); A. sumichrasti (Southern Mexico). The distinctive Edwards Plateau population in Texas, which was monophyletic in mtDNA except for one individual, should be studied in greater detail given habitat threat.

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Speciation and subsequent secondary contact in two edaphic endemic primroses driven by Pleistocene climatic oscillation.

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