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Gene Flow and Genetic Admixture Across a Secondary Contact Zone Between Two Divergent Lineages of the Eurasian Green Woodpecker Picusviridis J.-M

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Gene Flow and Genetic Admixture Across a Secondary Contact Zone Between Two Divergent Lineages of the Eurasian Green Woodpecker Picusviridis J.-M Gene flow and genetic admixture across a secondary contact zone between two divergent lineages of the Eurasian Green woodpecker Picusviridis J.-M. Pons, C. Masson, G. Olioso, J. Fuchs To cite this version: J.-M. Pons, C. Masson, G. Olioso, J. Fuchs. Gene flow and genetic admixture across a secondary contact zone between two divergent lineages of the Eurasian Green woodpecker Picusviridis. Wilson journal of ornithology, Wilson Ornithological Society, 2019, 160 (4), pp.935-945. 10.1007/s10336-019- 01675-6. hal-02861756 HAL Id: hal-02861756 https://hal.sorbonne-universite.fr/hal-02861756 Submitted on 9 Jun 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. 1 Gene flow and genetic admixture across a secondary contact zone between two divergent 2 lineages of the Eurasian Green woodpecker Picusviridis 3 4 5 6 Pons J.-M.*, Masson C.†,Olioso G.‡ and Fuchs J*. 7 8 *Département Systématique et Evolution, UMR7205 Institut de Systématique, Evolution, 9 Biodiversité CNRS MNHN UPMC EPHE, Sorbonne Universités, Muséum National 10 d’Histoire Naturelle, CP51, 57 rue Cuvier, F-75231 Paris Cedex 05, France 11 12 †63 rue des jonquilles 91210 Draveil 13 14 ‡Georges Olioso, 248 rue de l’industrie, Port-le-Nouvelle, 11210, France. 15 16 17 18 19 *Corresponding author: [email protected] 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 running title: gene flow across P. viridis contact zone 1 35 SUMMARY 36 Secondary contact zones are efficient natural systems to measure genetic differentiation and 37 gene flow and thus provide good opportunity to assess the level of reproductive isolation 38 between divergent evolutionary lineages. In this study, we used ten Z-linked and nine 39 autosomal loci from seven chromosomes and twenty males to evaluate gene flow across a 40 secondary contact zone between two mitochondrial lineages of the Eurasian Green 41 Woodpecker (Picus viridis), that diverged around one million years ago. One lineage 42 (sharpei) is distributed throughout the Iberian Peninsulawhereas the other one (viridis) is 43 widespread acrossthe Western Palearctic. These two lineages form a secondary contact zone 44 in southern France. Formerly treated as two subspecies of Picus viridis, several authors have 45 recently proposed to assign a specific rank to P. v. sharpei and P. v. viridis. Our results 46 indicate no introgression of nuclear loci in allopatric populationslocated on both sides ofthe 47 contact zone which thus actsas an efficient barrier to gene flow. All males sampledwithin the 48 contact zone and one male sampled near its eastern border were slightly admixed revealing 49 that reproductive isolation between sharpei and viridis is not completely achieved.In 50 accordance with the geographical range of each lineage, the two admixed males sampled near 51 the western border of the contact zone harboured a large proportion of sharpei alleles whereas 52 admixed males sampled eastwardlynear the Rhone Valley had a high proportion of viridis 53 alleles. Overall our results bring further support to consider sharpei and viridis as two 54 biological species. 55 56 57 58 59 KEYWORDS 60 Hybrid zone, introgression, clines, Z-linked loci,autosomal loci, gene flow, speciation, 61 Picusviridis. 2 62 ACKNOWLEDGEMENTS 63 We are very grateful to E. Garcia Franquesa and J. Quesada (Museu de Ciences Naturals, 64 Barcelona), G. Boano (Museo Civico di Storia Naturale di Carmagnola, Carmagnola), 65 E.Borgo (Museo di Storia Naturale di Genova, Genova), O. Llama Palacios and I. Rey Fraile 66 (Museo Nacional de Ciencas Naturales, Madrid) for sending us tissue samples. Sampling in 67 southern France was legally done under a CRBPO (Muséum national d’Histoire naturelle) 68 program directed by Georges Olioso. We thank Liviu Parau and one anonymous referee for 69 their helpful comments. The laboratory work was supported by the ‘Service de Systématique 70 Moléculaire’ (UMS 2700 OMSI, MNHN) and we thank C. Bonillo, D. Gey, J. Lambourdière 71 (UMS 2700) for their help. We also thank Ben Warren for his suggestions and help with 72 English. This work was funded by the UMR 7205, Institut de Systématique, Evolution, 73 Biodiversité. 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 3 90 INTRODUCTION 91 Zones of secondary contacts are very interesting for evolutionary biologists because they 92 provide unique opportunities to assess the level of reproductive isolation between closely 93 related taxa that have recently differentiated (Barton and Hewitt 1985). The limit between 94 intraspecific population divergence and interspecific divergence is often difficult to 95 hypothesize, especially when taxa are not in geographical contact. When taxa that have 96 evolved in allopatry meet each other in a secondary contact zone, it becomes possible to 97 safelytest their species status. Depending on the evolutionary history of both taxa and the 98 stage of completion of the speciation process, several scenarios are possible when they form a 99 secondary contact zone. If strong reproductive barriers have evolved in allopatry, both taxa 100 will not be able to form hybrids,and thus to mix their genomes when they come into 101 geographical contact. By contrast, if reproductive isolation is absent, bidirectional widespread 102 introgression erasesgeneticdivergence that evolved in allopatry, and eventually results in the 103 complete merging of parental genomes and disappearance of the contact zone(Endler 1977). 104 In case of recent divergence, however, reproductive barriers are often incomplete allowing 105 taxa to hybridize to a more or less extent (Barton and Hewitt 1985).Depending on the 106 efficiency of pre-zygotic (assortative mating) and post-zygotic reproductivebarriers (selection 107 against hybrids), we may expect that the movement of genes across the contact zoneis more or 108 less slowed down (Hewitt 1988). 109 By analyzing the geographical distribution of cytochrome b and Z-linked BRM intron-15 110 alleles in southern France, Spain and Europe, Pons et al. (2011)concluded that the Iberian and 111 the European lineages of the Eurasian Green Woodpecker (Picus viridis, Linneaus 1758) 112 came into secondary contact along thePyrenees chain and in the Languedoc-Roussillon region 113 along the Mediterranean coast.Pons et al. (2011) using molecular datingsuggested a mid- 114 Pleistocenesplit (~1 million years ago) between these two lineages, of which one isrestricted 4 115 to the Iberian Peninsula and southern France and the other is found over the rest of Europe up 116 to western Russia. According to Pons et al. (2011), allopatric divergence resulting from the 117 Pleistocene climatic oscillations isthe most probable scenario that would explain genetic 118 divergence of the Iberian population from the other one found elsewhere in Europe. 119 Both taxa differ by several plumage characters including the color of the face which is grey in 120 the Iberian Green woodpecker (sharpei lineage) and black in the Eurasian Green woodpecker 121 (viridis lineage) (Winkler and Christie 2019;Olioso and Pons 2011). Individuals with 122 intermediate plumage were mentioned at the beginning of the 20th century in the Languedoc- 123 Roussillon region (Jouard 1928) and are still currently observed (Olioso and Pons 2011). The 124 taxonomic treatment of the Iberian lineage varies according to taxonomic authorities and is 125 considered either as a species (Picus sharpei, H. Saunders, 1872) (Perktas et al. 2011; Gill and 126 Donsker 2018; Del Hoyo et al. 2019) or a subspecies (Picus viridis sharpei) (Dickinson and 127 Moore 2013). 128 In this study, we assess gene flow and genetic introgression between sharpei and viridis 129 across the Mediterranean secondary contact zone withten Z-linked loci and nine autosomal 130 loci using Bayesian inference of genetic population structure and spatial variation in alleles’ 131 frequencies. 132 Our primary aims are:(1) to test whether the secondary contact zone acts as an efficient barrier 133 to the eastward moving of sharpei alleles and the westward moving of viridis alleles and (2) 134 to assess the level of genetic admixture within the contact zone. 135 METHODS 136 Sampling design 137 Two allopatric populations were sampled for each lineage and one population was sampled 138 across the contact zone in southern France. According to their distances from the contact 139 zone, populations which were oriented along a South-West/North-East transect were referred 5 140 as close allopatric populations, populations 2 and 4 (Catalonia and Provence, Fig. 1), or 141 distant allopatry, populations 1 and 5 (Central Spain and North-West Italy, Fig. 1). Within 142 each population, four males were chosen at different localities that were several kilometers 143 apart (Fig. 1, Table S1). The studied contact zone (population 3) reported on Fig. 1 has been 144 delimited after Pons et al. (2011) and Olioso and Pons (2011) as the area where the two 145 mitochondrial lineages overlap and where birds with intermediate plumage are encountered. 146 Across the contact zone, four males were sampled so as to be widely distributed from the 147 western side of the contact zoneup to the eastern border (Fig. 1). Tissues (muscles) from 148 allopatric populations 1, 2 and 5 were obtained through loans from the Museo Nacional de 149 Ciencias Naturale (Madrid), Museu de Ciències Naturals de Barcelona, Museo di Storia 150 Naturale di Genova, a n d Museo Civico di storia naturale di Carmagnola (Table S1).
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