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Gene flow and genetic admixture across a secondary contact zone between two divergent lineages of the Eurasian Green Woodpecker Picus viridis

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Abstract

Secondary contact zones are natural systems which can be efficiently used to measure genetic differentiation and gene flow and thus provide a good opportunity to assess the level of reproductive isolation between divergent evolutionary lineages. In this study, we used ten Z-linked and nine autosomal loci from seven chromosomes and twenty males to evaluate gene flow across a secondary contact zone between two mitochondrial lineages of the Eurasian Green Woodpecker (Picus viridis), that diverged around 1 million years ago. One lineage (Picus viridissharpei) is distributed throughout the Iberian Peninsula whereas the other one (Picus viridisviridis) is widespread across the Western Palearctic. These two lineages form a secondary contact zone in southern France. Formerly treated as two subspecies of Picus viridis, several authors have recently proposed assigning a specific rank to P. viridis sharpei and P. viridis viridis. Our results indicate no introgression of nuclear loci in allopatric populations located on both sides of the contact zone, which thus acts as an efficient barrier to gene flow. All males sampled within the contact zone and one male sampled near its eastern border were slightly admixed revealing that reproductive isolation between P. viridissharpei and P viridis viridis has not been completely achieved. In accordance with the geographical range of each lineage, the two admixed males sampled near the western border of the contact zone harboured a large proportion of P. viridissharpei alleles whereas admixed males sampled eastwardly near the Rhone Valley had a high proportion of P. viridis viridis alleles. Overall our results further support considering P. viridissharpei and P. viridisviridis as two biological species.

Zusammenfassung

Genfluss und genetische Vermischung entlang einer sekundären Kontaktzone zwischen zwei getrennten Abstammungslinien des Grünspechts Picus viridis.

Sekundäre Kontaktzonen sind wirkungsvolle natürliche Systeme zur Messung von genetischer Differenzierung und Genfluss und bieten so eine gute Möglichkeit, das Ausmaß der reproduktiven Isolation zwischen getrennten evolutionären Abstammungslinien zu bewerten. In dieser Studie untersuchten wir anhand von zehn an das Z-Chromosom gekoppelten und neun autosomalen Genloci von sieben Chromosomen aus einer Stichprobe von 20 Männchen den Genfluss über eine sekundäre Kontaktzone zwischen zwei mitochondrialen Linien des Grünspechts Picus viridis, welche sich vor etwa einer Million Jahre auseinanderentwickelt haben. Eine Linie (sharpei) kommt auf der gesamten Iberischen Halbinsel vor, während die andere (viridis) in der Westpaläarktis weit verbreitet ist, wobei beide in Südfrankreich eine sekundäre Kontaktzone ausbilden. Früher wurden die beiden als zwei Unterarten von Picus viridis betrachtet, in neuerer Zeit haben jedoch verschiedene Autoren angeregt, P. v. sharpei und P. v. viridis in den Artstatus zu erheben. Unsere Ergebnisse zeigen keine Introgression nukleärer Loci bei allopatrischen Populationen auf beiden Seiten der Kontaktzone, welche somit eine wirkungsvolle Barriere für den Genfluss darstellt. Sämtliche in der Kontaktzone beprobten Männchen sowie ein Männchen aus der Nähe ihrer östlichen Grenze hatten geringfügige Beimischungen, was belegt, dass noch keine vollständige reproduktive Isolation zwischen sharpei und viridis erreicht ist. Übereinstimmend mit der geografischen Verbreitung der jeweiligen Abstammungslinie besaßen „Misch“-Männchen aus der Nähe der westlichen Grenze der Kontaktzone einen höheren Anteil an sharpei–Allelen, wohingegen weiter östlich nahe des Rhonetals beprobte „Misch“-Männchen einen hohen Anteil viridis-Allele aufwiesen. Insgesamt lieferten unsere Ergebnisse weitere Argumente für die Einstufung von sharpei und viridis als zwei biologische Arten.

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Acknowledgements

We are very grateful to E. Garcia Franquesa and J. Quesada (Museu de Ciences Naturals, Barcelona), G. Boano (Museo Civico di Storia Naturale di Carmagnola, Carmagnola), E. Borgo (Museo di Storia Naturale di Genova, Genova), O. Llama Palacios and I. Rey Fraile (Museo Nacional de Ciencas Naturales, Madrid) for sending us tissue samples. Sampling in southern France was legally done under a CRBPO (Muséum national d’Histoire naturelle) program directed by Georges Olioso. We thank Liviu Parau and one anonymous referee for their helpful comments. The laboratory work was supported by the Service de Systématique Moléculaire (UMS 2700 OMSI, MNHN), and we thank C. Bonillo, D. Gey, J. Lambourdière (UMS 2700) for their help. We also thank Ben Warren for his suggestions and help with the English language. This work was funded by UMR 7205, Institut de Systématique, Evolution, Biodiversité.

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Correspondence to J.-M. Pons.

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Fig. S1 Phenotypes of the three adult males included in the study (DOCX 467 kb)

10336_2019_1675_MOESM2_ESM.docx

Fig. S2a Maximum-likelihood clines obtained with hzar for 16 autosomal alleles (eight loci) fitting the cline model. S2b Maximum-likelihood clines obtained with HZAR for 18 Z-linked alleles (seven loci) fitting the cline model (DOCX 147 kb)

10336_2019_1675_MOESM3_ESM.docx

Fig. S3 Relative abundance estimates of Picus viridis obtained from the Monitoring Common Birds in France program managed by the Centre de Recherches par le Baguage des Populations d’Oiseaux, Muséum national d’Histoire naturelle (DOCX 519 kb)

Table S1 Information on populations, individuals and tissues (XLSX 10 kb)

Table S2 Information on loci and primers (XLSX 13 kb)

10336_2019_1675_MOESM6_ESM.xlsx

Table S3 Cline model parameters and values of Akaike information criterion corrected for small sample sizes (cline model vs. null model) for each Z-linked and autosomal allele (XLSX 26 kb)

Table S4 Allelic frequencies for each Z-linked and autosomal locus (XLSX 27 kb)

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Pons, JM., Masson, C., Olioso, G. et al. Gene flow and genetic admixture across a secondary contact zone between two divergent lineages of the Eurasian Green Woodpecker Picus viridis. J Ornithol 160, 935–945 (2019). https://doi.org/10.1007/s10336-019-01675-6

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