Després, L., Henniaux, C., Rioux, D., Capblancq, T., Zupan, T.Č
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applyparastyle "body/p[1]" parastyle "Text_First" Biological Journal of the Linnean Society, 2019, 126, 95–113. With 6 figures. Downloaded from https://academic.oup.com/biolinnean/article-abstract/126/1/95/5214084 by Divisione Coordinamento Biblioteche Milano user on 30 January 2019 Inferring the biogeography and demographic history of an endangered butterfly in Europe from multilocus markers LAURENCE DESPRÉS1*, CLÉMENT HENNIAUX1, DELPHINE RIOUX1, THIBAUT CAPBLANCQ1, SARA ZUPAN2, TATJANA ČELIK3, MARCIN SIELEZNIEW4, LUCIO BONATO5 and GENTILE FRANCESCO FICETOLA1,6 1Université Grenoble Alpes, LECA UMR5553, CNRS, F-38000 Grenoble, France 2University of Primorska, Faculty of Mathematics, Natural Sciences and Information Technologies, Glagoljaška 8, SI-6000 Koper, Slovenia 3Research Centre of the Slovenian Academy of Sciences and Arts, Jovan Hadži Institute of Biology, Novi trg 2, SI-1000 Ljubljana, Slovenia 4Laboratory of Insect Evolutionary Biology and Ecology, Institute of Biology, University of Bialystok, 15- 245 Białystok, Poland 5Department of Biology, Università degli Studi di Padova, Padova, Italy 6Department of Environmental Science and Policy, Università degli Studi di Milano, Milano, Italy Received 5 June 2018; revised 25 September 2018; accepted for publication 26 September 2018 The genetic structure of a species is influenced by its history and by current gene flow. Using a population genomics approach, we infer the demographic history of the false ringlet (Coenonympha oedippus) in Europe based on 1594 genome-wide double digest restriction site associated DNA sequencing loci from 96 individuals (32 localities) sam- pled throughout the fragmented species range. In contrast to the weak geographical structure in mitochondrial DNA, a clear nuclear differentiation was observed between the westernmost Atlantic localities, those from the western Alps and all other sampled localities. Mountain ridges were the main factor explaining population divergence at the European scale, while isolation by distance was found at a regional scale. We applied Approximate Bayesian Computation in a coalescent framework to infer past and contemporary demographic parameters. The best scenario suggested a first divergence between French and all other European populations around 66 000 years ago, such that the species survived the Last Glacial Maximum in at least two distinct areas separated by the Alps. This scenario fits species distribution modelling identifying variation of suitable areas with past climatic modifications. The Atlantic and western Alps lineages separated about 6000 years ago. Strong population decline was inferred in these lineages during historical time, in agreement with multiple records of recent decline of this species in Europe. ADDITIONAL KEYWORDS: Coenonympha oedippus – ddRADseq – demographic history – genetic diversity – glacial refuges – mtDNA – population size – species distribution modelling. INTRODUCTION conservation biology for decades. The Pleistocene cold periods in the northern hemisphere have influenced The genetic structure of a species reflects both its history the distribution of species with range fluctuations and ongoing gene flow. Characterizing demographic linked to climatic variations. During glaciations, many histories and identifying the main environmental temperate European taxa were restricted to southern factors shaping genetic variation at different spatial ice-free refuges (Taberlet et al., 1998). The present scales have been a major focus in evolutionary and distribution of most species in Europe has resulted from a northward recolonization from those southern *Corresponding author. E-mail: laurence.despres@univ-greno- refuges after the Last Glacial Maximum (LGM), about ble-alpes.fr 21 kya (Strandberg et al., 2011). Under this hypothesis, © 2018 The Linnean Society of London, Biological Journal of the Linnean Society, 2019, 126, 95–113 95 96 L. DESPRÉS ET AL. the southern part of Europe should present the highest as a consequence of human activities (Lhonore & genetic diversity, in contrast to the recently recolonized Lagarde, 1999). Despite the wide distribution range of northern part (Besold et al., 2008; Patricelli et al., 2013). this butterfly, from Atlantic to Pacific coasts, very little Downloaded from https://academic.oup.com/biolinnean/article-abstract/126/1/95/5214084 by Divisione Coordinamento Biblioteche Milano user on 30 January 2019 However, genetic analyses have identified numerous information is available on the intraspecific pattern additional extra-mediterranean refuges, thus strongly of genetic diversity in C. oedippus, and on the genetic modifying the biogeographical view of Europe (Schmitt connections between populations. Coenonympha & Varga, 2012). This picture is complicated in species oedippus is generally considered to be a monotypic with a wide Eurasian distribution, where other potential species, despite many subspecific and infrasubspecific eastern refuges could have existed, with possible taxa proposed by different taxonomists (Bozano, 2002), admixture occurring between diverging lineages although genetic studies have often found cryptic during post-glacial recolonization (Grassi et al., 2008). genetic structure within butterfly species (Hebert Geographical distribution and genetic structure are et al., 2004; Dincă et al., 2011, 2015; Ritter et al., 2013; affected not only by the evolutionary history of species Lavinia et al., 2017). but also by dispersal abilities, present demographic We used double digest restriction site-associated characteristics – especially fluctuations in population DNA sequencing (ddRADseq) to identify thousands of size – and by habitat fragmentation (Keyghobadi, 2007; genetic markers without any prior knowledge on the Louy et al., 2013). Many lowland insect species have genome of Coenonympha (Peterson et al., 2012). We been particularly affected by human impact via the used nuclear genetic diversity to test for alternative intensification of agriculture (insecticide spraying, land demographic histories (splits, expansions, recent draining). Although they were abundant a few decades declines) of European populations by an Approximate ago, they now show highly fragmented populations Bayesian Computation (ABC) approach in a coalescent with high extinction risk (Hallmann et al., 2017). framework. Finally, we performed species distribution Analyses of genetic diversity within and between modelling (MaxEnt) to identify current and past populations provide key information for conservation climatically suitable areas for C. oedippus in Europe. of endangered species given that they allow us to infer important demographic parameters such as historical and contemporary effective population sizes, dispersal MATERIAL AND METHODS rates across populations and levels of consanguinity. This knowledge is necessary to guide conservation STUDY SPECIES actions such as the creation of corridors favouring the Coenonympha oedippus (Fabricius, 1787) (Lepidoptera: natural re-colonization of suitable habitats, or the best Nymphalidae) is a univoltine Palearctic sedentary choice of individuals for a successful re-location. To species flying mainly in June and July (Čelik et al., date, most phylogeographical studies at the continental 2009; Verovnik et al., 2012; Bonato et al., 2014). It is scale have been based on mitochondrial DNA (mtDNA), a hygrophilous insect inhabiting mostly wet meadows and population genetic analysis have focused on a few and fens, where caterpillars feed on Carex spp. as well allozyme or microsatellite markers and required the as on Molinia caerulea, but at the southern range limit analysis of many individuals per population, which in north-eastern Italy and Slovenia it can be found also was not always possible for endangered species. With on drier grasslands (Habeler, 1972; Čelik et al., 2015). the development of high-throughput sequencing Coenonympha oedippus is one of the most endangered technologies, it is now possible to infer the genetic butterfly species in Europe and is listed in Annexes II diversity within and between populations with only and IV of the Habitats Directive as well in Appendix a few individuals per population, because the low II of the Bern Convention (Van Swaay et al., 2010). It number of individuals sampled is partly compensated became extinct in three of the 14 countries where it for by a very high number of loci genotyped (Nazareno had been recorded (Van Swaay & Warren, 1999), i.e. et al., 2017). in Slovakia (Pastoralis & Reiprich, 1995), Bulgaria In this study we used high-throughput genotyping (Staub & Aistleitner, 2006) and Switzerland (Dušej besides the classical mitochondrial barcode (partial et al., 2010). In most of other countries C. oedippus is CO1) to uncover the past and current factors involved declining and in the last 100 years it has disappeared in shaping the genetic structure of one of the most from many localities, e.g. in Germany, where only endangered butterfly species in Europe, the false one meta-population is still present in Bavaria (Bräu ringlet (Coenonympha oedippus). Although the species et al., 2010), and France (Lhonore & Lagarde, 1999), is distributed across Eurasia from western France where the species went extinct in the Paris region, to Japan (Bozano, 2002), its range is today highly and is currently present in only two disconnected and fragmented, especially throughout Europe (Kudrna distant regions: between the Atlantic coast and the et al., 2015), because its habitat (mainly