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Joint analysis of microsatellites and flanking sequences enlightens complex demographic history of interspecific gene flow and vicariance in rear-edge oak populations

Abstract

Inference of recent population divergence requires fast evolving markers and necessitates to differentiate shared genetic variation caused by ancestral polymorphism and gene flow. Theoretical research shows that the use of compound marker systems integrating linked polymorphisms with different mutational dynamics, such as a microsatellite and its flanking sequences, can improve estimation of population structure and inference of demographic history, especially in the case of complex population dynamics. However, empirical application in natural populations has so far been limited by lack of suitable methods for data collection. A solution comes from the development of sequence-based microsatellite genotyping which we used to study molecular variation at 36 sequenced nuclear microsatellites in seven Quercus canariensis and four Q. faginea rear-edge populations across Algeria. We aim to decipher their taxonomic relationship, past evolutionary history and recent demographic trajectory. First, we compare the estimation of population genetics parameters and simulation-based inference of demographic history from microsatellite sequence alone, flanking sequence alone or the combination of linked microsatellite and flanking sequence variation. Second, we apply random forest approximate Bayesian computation to identify which of these sequence types is most informative. Whereas analysing microsatellite variation alone indicates recent interspecific gene flow, additional information gained by integrating nucleotide variation in flanking sequences, by reducing homoplasy, suggests ancient interspecific gene flow followed by drift in isolation instead. The weight of each polymorphism in the inference also demonstrates the value of linked variations with contrasted mutation dynamic to improve estimation of both demographic and mutational parameters.

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Fig. 1: Geographical context and population genetic structure of Quercus faginea and Q. canariensis Algerian populations.
Fig. 2: Description of simulated models of Q. faginea and Q. canariensis Algerian populations demographic history.
Fig. 3: Genetic diversity of Q. faginea (S02, S03, S08, S11) and Q. canariensis (S01, S04, S05, S06, S07, S09, S10) Algerian populations.
Fig. 4: Contribution of different types of polymorphism measured as Variable Importance (y-axis).

Data availability

The datasets of Q. faginea and Q. canariensis genotypes used in this study are available in Dryad (https://doi.org/10.5061/dryad.8cz8w9gth).

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Acknowledgements

We thank Rémy Petit and Cecile Bacles for advice and comments on a previous versions of the manuscript. Sequence-based microsatellite genotyping was performed at the PGTB (doi:10.15454/1.5572396583599417E12) with the help of Emilie Chancerel and Erwan Guichoux. Computer time for the demographic simulations and ABC inferences was provided by the computing facilities MCIA (Mésocentre de Calcul Intensif Aquitain) of the Université de Bordeaux and of the Université de Pau et des Pays de l’Adour. We are grateful to the Editor and three anonymous reviewers for their suggestions that greatly improved the manuscript.

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AA, EV, YB and OL obtained the funding for the research, contributed to the design of the study and the interpretation of the results. AA performed the sampling and collected field data under the supervision of YB. AA and OL performed DNA extraction. OL performed the laboratory work to produce the sequencing data, the bioinformatic and population genetic data analysis, drafted the first version of the manuscript and handled the manuscript submission and revisions. All authors contributed to the article revisions and approved the final version.

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Correspondence to Olivier Lepais.

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Lepais, O., Aissi, A., Véla, E. et al. Joint analysis of microsatellites and flanking sequences enlightens complex demographic history of interspecific gene flow and vicariance in rear-edge oak populations. Heredity (2022). https://doi.org/10.1038/s41437-022-00550-0

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