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Genomic data and multi-species demographic modelling uncover past hybridization between currently allopatric freshwater species

Abstract

Evidence for ancient interspecific gene flow through hybridization has been reported in many animal and plant taxa based on genetic markers. The study of genomic patterns of closely related species with allopatric distributions allows the assessment of the relative importance of vicariant isolating events and past gene flow. Here, we investigated the role of gene flow in the evolutionary history of four closely related freshwater fish species with currently allopatric distributions in western Iberian rivers—Squalius carolitertii, S. pyrenaicus, S. torgalensis and S. aradensis—using a population genomics dataset of 23,562 SNPs from 48 individuals, obtained through genotyping by sequencing (GBS). We uncovered a species tree with two well-differentiated clades: (i) S. carolitertii and S. pyrenaicus; and (ii) S. torgalensis and S. aradensis. By using D-statistics and demographic modelling based on the site frequency spectrum, comparing alternative demographic scenarios of hybrid origin, secondary contact and isolation, we found that the S. pyrenaicus North lineage is likely the result of an ancient hybridization event between S. carolitertii (contributing ~84%) and S. pyrenaicus South lineage (contributing ~16%), consistent with a hybrid speciation scenario. Furthermore, in the hybrid lineage, we identify outlier loci potentially affected by selection favouring genes from each parental lineage at different genomic regions. Our results suggest that ancient hybridization can affect speciation and that freshwater fish species currently in allopatry are useful to study these processes.

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Fig. 1: Distribution range of the four Squalius species in Portuguese rivers and sampling locations.
Fig. 2: Global patterns of genetic differentiation.
Fig. 3: Unrooted species tree graph obtained with TreeMix.
Fig. 4: D-statistics calculated for different topologies.
Fig. 5: Schematic representation of the likelihood of the models tested with fastsimcoal2.
Fig. 6: Outlier loci detected in S. pyrenaicus North.

Data availability

The catalog, datasets and scripts used are available from the Dryad Digital Repository https://doi.org/10.5061/dryad.v15dv41wk. Sequencing files (bam files for all individuals) are deposited on the Sequence Read Archive (SRA) under BioProject PRJNA751527.

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Acknowledgements

We thank Tiago F. Jesus for the help in sample preparation. We also thank three anonymous reviewers and the associate editor for constructive comments on previous versions of the manuscript. This work was funded by strategic projects UID/BIA/00329/2013 (2015–2018) and UIDB/00329/2020 granted to cE3c from the Portuguese National Science Foundation—Fundação para a Ciência e a Tecnologia (FCT). SLM is funded by an FCT scholarship (SFRH/BD/145153/2019). VCS was funded by FCT (CEECIND/02391/2017 and CEECINST/00032/2018/CP1523/CT0008) and by EU H2020 program (Marie Skłodowska-Curie grant 799729). We thank the INCD (https://incd.pt/) for use of their computing infrastructure, which is funded by FCT and FEDER (project 01/SAICT/2016 n° 022153).

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MMC and VCS conceived and designed the study; MPM performed laboratory work; SLM and VCS analyzed the data; SLM, VCS, and MMC wrote the manuscript. All authors contributed to the drafts and gave final approval for publication.

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Correspondence to Vitor C. Sousa.

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Mendes, S.L., Machado, M.P., Coelho, M.M. et al. Genomic data and multi-species demographic modelling uncover past hybridization between currently allopatric freshwater species. Heredity 127, 401–412 (2021). https://doi.org/10.1038/s41437-021-00466-1

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