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Genetic Structure Among Remnant Populations of a Migratory Passerine, the Northern Wheatear Oenanthe Oenanthe

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Genetic Structure Among Remnant Populations of a Migratory Passerine, the Northern Wheatear Oenanthe Oenanthe Ibis (2016), 158, 857–867 Genetic structure among remnant populations of a migratory passerine, the Northern Wheatear Oenanthe oenanthe H. HERMAN VAN OOSTEN,1,2* JAKOB C. MUELLER,3 JENTE OTTENBURGHS,4 CHRISTIAAN BOTH5 & BART KEMPENAERS3 1Oenanthe Ecologie, Hollandseweg 42, Wageningen, 6706 KR, The Netherlands 2Department of Animal Ecology & Ecophysiology, Institute for Water and Wetland Research, Radboud University, PO Box 9010, Nijmegen, 6500 GL, The Netherlands 3Department of Behavioural Ecology & Evolutionary Genetics, Max Planck Institute for Ornithology, Seewiesen, Germany 4Resource Ecology Group, Wageningen University, Droevendaalsesteeg 3a, Wageningen, 6708 PB, The Netherlands 5Animal Ecology Group, Center for Ecological and Evolutionary Studies, University of Groningen, PO Box 11103, Groningen, 9700 CC, The Netherlands Continuous animal populations often become fragmented due to anthropogenic habitat alterations. These small, fragmented populations are fragile due to demographic and genetic factors, whereas immigration can enhance their long-term viability. Previously, we showed that high philopatry affected the local dynamics of three small and remnant subpopulations of Northern Wheatears in The Netherlands. Here, we show that these three populations together with an additional larger population in the European lowlands are highly genetically differentiated based on 22 microsatellite markers. In contrast, we found no evidence for differentiation using two mitochondrial DNA markers. An IMa2 analysis indicates that gene flow has occurred regularly among our sampled populations. As immigration of colour-ringed birds among our sampled populations is rare at best, our results suggest that the populations have recently become isolated from one another. Low dispersal rates in highly mobile birds may occur when suitable habitat becomes highly fragmented, and will accentuate stochastic demographic processes and inbreeding, both reducing population viability. As dispersal rates are low among populations of Northern Wheatears in The Netherlands, there is only a small probability of recoloniza- tion of habitat patches where populations have become locally extinct. Keywords: FST, gene flow, genetic drift, genetic structuring, heterozygosity, IMa2, microsatellite, mtDNA, philopatry, songbird. Due to a variety of anthropogenic influences, most against stochastic population fluctuations and prominently habitat destruction, populations once against loss of genetic diversity through genetic distributed continuously may become fragmented, drift and inbreeding (Brown & Kodric-Brown persisting in isolation of each other. These popula- 1977, Slatkin 1987, Frankham 1996). Connectivity tions are at risk of extinction because of demo- of populations can be determined both demo- graphic and genetic factors (Gilpin & Soule 1986). graphically and genetically, with each method hav- Exchange between populations is important for ing its own merits and shortcomings (Lowe & the long-term persistence of small populations Allendorf 2010). Demographic connectivity, (Hanski & Gilpin 1997, Hanski 1998): it buffers defined as the degree to which population growth and vital rates are influenced by exchange between *Corresponding author. populations, is a function of the relative contribu- Email: [email protected] tion of immigration to population growth. Genetic © 2016 British Ornithologists’ Union 858 H. H. van Oosten et al. connectivity, defined as ‘the degree to which gene continuous population in the coastal dunes and a flow influences evolutionary processes in popula- more isolated population inland (Teixeira 1979, tions’ (Lowe & Allendorf 2010), is mainly a func- Sovon 2002; Fig. 1). Dispersal was probably more tion of the absolute number of effective frequent (as is often the case in more continuous immigrants (Waples & Gaggiotti 2006), defined as populations; Wiens 1995) and demographic isola- breeding individuals that contribute offspring to tion may not have resulted in genetic structuring, the next generation. For conservation purposes we although the possibility exists that the coastal and need information on both demographic and inland populations were separated to some extent. genetic connectivity to make inferences about the At present, limited immigration may still maintain potential persistence of populations. sufficient gene flow between seemingly isolated Previously we showed, using an Integrated Pop- populations of this declining species, as has been ulation Model, that the small relict populations of shown for migratory and philopatric passerines that Northern Wheatear Oenanthe oenanthe in The show little genetic structuring among contemporary Netherlands have high philopatry, and that sub- fragmented populations (Cerulean Warbler Seto- population dynamics were to a varying degree phaga cerulea, Veit et al. 2005, Golden-cheeked determined by local population processes (Van Warbler Setophaga chrysoparia, Lindsay et al. Oosten et al. 2015). These local relict populations 2008). Other long-distance migratory species with constitute an estimated 50% of the breeding large ranges (e.g. European Pied Flycatcher Ficedula Northern Wheatears in The Netherlands, and hypoleuca, Lehtonen et al. 2009, Barn Swallow Hir- intensive colour-ringing allowed estimation of all undo rustica, Santure et al. 2010, Eurasian Reed demographic parameters with high accuracy. The Warbler Acrocephalus scirpaceus, Prochazka et al. estimated and observed low levels of immigration 2011) show little genetic differentiation over most and small population sizes may quickly lead to of their breeding ranges, suggesting appreciable genetic differentiation as a result of genetic drift levels of dispersal in these highly mobile species. and rapid fixation of alternate alleles among iso- This paper aims to describe the level of genetic lated populations. differentiation between four discrete remnant pop- In The Netherlands, Northern Wheatears had a ulations of Northern Wheatears. We use large breeding range 25 years ago, with a large microsatellite and mitochondrial DNA (mtDNA) D C A A A D D C C R 1973-77 2010 Figure 1. Breeding distribution of Northern Wheatears in the Netherlands in 1973–77 (left; Teixeira 1979) and 2010 (right; Boele et al. 2012). The three research sites are denoted with capital letters (see text) and the arrow indicates the island of Ameland from where additional DNA was sampled for mtDNA analysis. Dots and squares refer to different number of territories per 5-km square. The inset shows the location of the four sites in Northwestern Europe. Maps courtesy of Sovon. © 2016 British Ornithologists’ Union Genetic structure in Northern Wheatear populations 859 marker data to test three alternative predictions felled trees. Individuals forage mostly on the about genetic variation. ground, hunting for beetles, beetle larvae and cater- pillars (Van Oosten et al. 2014). Large expanses of 1 Geographically isolated Northern Wheatear breeding habitat were lost due to eutrophication populations show no genetic structure, because and acidification, which stimulated growth of tall there is sufficient gene flow or because the sep- grasses (Bobbink et al. 2010). This rendered suitable aration is too recent. Genetic variation is simi- short grown grasslands into inaccessible stands of tall lar across the populations. grasses, including species such as Wood Small-reed 2 Recent isolation and genetic drift have already Calamagrostis epigejos, Sand Sedge Carex arenaria resulted in the development of population and Marram Grass Ammophila arenaria. genetic structure. In this case, we predict that We collected DNA of Northern Wheatear nest- populations differ with respect to their lings at four sites: three in the Netherlands (Cas- mtDNA but not (yet) nuclear microsatellites, tricum (C), Den Helder (D), Aekingerzand (A)) because effective population size of mtDNA and one in Germany (Rhineland-Palatinate (R)) markers is only one-quarter that of the nuclear (Fig. 1) between 2006 and 2013. The coastal popu- microsatellite markers. Due to drift processes, lation Castricum (site C, 7–24 breeding pairs genetic variation may be lower in the smaller 2007–2013, also present more than 200 years ago; populations compared with a larger German Nozeman 1789) is separated by 35 km from the population in the Rhineland-Palatinate. coastal population Den Helder (site D, 47–74 3 Past selection on birds breeding in different breeding pairs 2007–2013). The inland population habitats (see below) has led to more ancient iso- at Aekingerzand (site A, 11–47 breeding pairs lation and the formation of genetically widely 2007–2013) is 110 km from the Castricum popula- differing sub-populations. In this case, we expect tion and 125 km from the Den Helder population. strong population structure, both in microsatel- Individuals from populations C and D breed in lites and in mtDNA, with a likely separation coastal dunes within 1 km of the sea, whereas indi- between the coastal and inland populations. viduals from population A breed in heathland with To differentiate between these hypotheses, we drift sands. The German population near Bad analysed 22 nuclear microsatellite markers and two Durkheim,€ Rhineland-Palatinate (site R, 100 breed- mtDNA markers. The mtDNA markers have been ing pairs), consists of individuals that breed mostly used to distinguish between (sub)species within in vineyards (Buchmann 2001) and is approxi- the genus Oenanthe (Aliabadian et al. 2007) and mately 400 km from the three Dutch populations.
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