Variable levels of introgression between the endangered Podarcis carbonelli and highly divergent congeneric species

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Abstract

Recent empirical studies have demonstrated that speciation with gene flow is more common than previously thought. From a conservation perspective, the potential negative effects of hybridization raise concerns on the genetic integrity of endangered species. However, introgressive hybridization has also been growingly recognized as a source of diversity and new advantageous alleles. Carbonell’s wall lizard (Podarcis carbonelli) is an endangered species whose distribution overlaps with four other congeneric species. Our goal here was to determine whether P. carbonelli is completely reproductively isolated from its congeners and to evaluate the relevance of hybridization and interspecific gene flow for developing a conservation plan. We used restriction site associated DNA (RAD) sequencing to discover SNPs in samples from four contact zones between P. carbonelli and four other species. Principal component analysis, multilocus genotype assignment and interspecific heterozygosity suggest incomplete reproductive isolation and ongoing gene flow between species. However, hybridization dynamics vary across all pairs, suggesting complex interactions between multiple intrinsic and extrinsic barriers. Despite seemingly ubiquitous interspecific gene flow, we found evidence of strong reproductive isolation across most contact zones. Instead, indirect effects of hybridization like waste of reproductive effort in small isolated populations may be more problematic. Our results highlight the need to further evaluate the consequences of introgression for P. carbonelli, both on a geographic and genomic level and included in a comprehensive and urgently needed conservation plan. Besides, those findings will add important insights on the potential effects of hybridization and introgression for endangered species.

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Fig. 1: Distribution of each Podarcis species in Iberian Peninsula, the location of sampled contact zones and reference populations analyzed.
Fig. 2: Principal Component Analysis (PCA) of SNP variation.
Fig. 3: Analysis of genetic variability and admixture performed with SNP data.
Fig. 4: Overall genotypic composition for each contact zone.

Data availability

Raw sequence reads from ddRAD-seq are deposited in the NCBI Sequence Read Archive (SRA). The BioProject accession number is PRJNA665746. VCF files with the complete datasets for each contact zone have been deposited on DRYAD (https://doi.org/10.5061/dryad.k0p2ngf51).

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Acknowledgements

We thank E. Pérez, M. A. Carretero, C. Rato, A. Perera, V. Gomes, N. Sillero, A. Crotini and A. Žagar for helping with sample collection. We also thank B. Gernster for the manuscript revision. This study benefited from the Montpellier Bioinformatics Biodiversity platform supported by the LabEx CeMEB, an ANR “Investissements d’avenir” program (ANR-10-LABX-04-01). GCD was supported by a PhD grant (SFRH/BD/89750/2012), and AK and CP by IF contracts (IF/00641/2014/CP1256/CT0008 and IF/01597/2014/CP1256/CT0009, respectively) under the Programa Operacional Potencial Humano—Quadro de Referência Estratégico Nacional funds from the European Social Fund and Portuguese Ministério da Educação e Ciência and PAC by the ANR grant ANR-19-CE02-0011 – IntroSpec. Support was also provided by national funds through FCT projects: PTDC/BIA-BEC/102179/2008 – FCOMP-01-0124-FEDER-007062, under FEDER COMPETE funds; PTDC/BIA-EVL/28090/2017 – POCI-01-0145-FEDER-028090 and PTDC/BIA-EVL/30288/2017 – NORTE-01-0145-FEDER-30288 co-funded by NORTE2020 through Portugal 2020 and FEDER Funds. Specimens for this study were captured and handled under permit numbers 119 to 124/2013/CAPT and 486 to 490/2014/CAPT by Instituto da Conservação da Natureza e das Florestas (ICNF, Portugal) and permit 201318800014253 by Junta de Andalucía, Consejería de Agricultura, Pesca y Medio Ambiente (Spain).

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  1. These authors contributed equally: Pierre-André Crochet, Catarina Pinho

Affiliations

  1. Centro de Investigação em Biodiversidade e Recursos Genéticos, CIBIO/InBIO, Universidade do Porto, Vairão, Portugal

    Guilherme Caeiro-Dias, Antigoni Kaliontzopoulou, Mariana Meneses-Ribeiro & Catarina Pinho

  2. Departamento de Biologia, Faculdade de Ciências, Universidade do Porto, Porto, Portugal

    Guilherme Caeiro-Dias

  3. CEFE, CNRS, Université de Montpellier, EPHE, IRD, Université Paul Valéry Montpellier 3, Montpellier, France

    Guilherme Caeiro-Dias & Pierre-André Crochet

  4. Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland

    Alan Brelsford

  5. Biology Department, University of California Riverside, Riverside, CA, USA

    Alan Brelsford

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  1. Guilherme Caeiro-Dias
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Caeiro-Dias, G., Brelsford, A., Kaliontzopoulou, A. et al. Variable levels of introgression between the endangered Podarcis carbonelli and highly divergent congeneric species. Heredity (2020). https://doi.org/10.1038/s41437-020-00386-6

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