Abstract
Black grouse (Tetrao tetrix) in Central Europe have undergone a severe contraction of their range in recent decades with only a few small isolated remaining populations. Here we compare genetic diversity of two contemporary isolated populations (Sallandse Heuvelrug, Netherlands and Lüneburger Heide, Germany) with historical samples from the same region collected within the last one hundred years. We use markers with both putatively neutral and functional variation to test whether the present small and highly fragmented populations hold lower genetic diversity compared to the former larger population. For this we applied three different types of genetic markers: nine microsatellites and 21 single nucleotide polymorphisms (SNPs), both sets which have been found to be neutral, and two functional major histocompatibility complex (MHC) genes for which there is evidence they are under selection. The contemporary small isolated populations displayed lower neutral genetic diversity compared to the corresponding historical samples. Furthermore, samples from Denmark showed that this now extinct population displayed lower genetic variation in the period immediately prior to the local extinction. Population structure was more pronounced among contemporary populations compared to historical populations for microsatellites and SNPs. This effect was not as distinct for MHC which is consistent with the possibility that MHC has been subjected to balancing selection in the past, a process which maintains genetic variation and may minimize population structure for such markers. Genetic differentiation among the present populations highlights the strong effects of population decline on the genetic structure of natural populations, which can be ultimately attributed to habitat loss following anthropogenic land use changes.
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References
Arguello JR, Little AM, Pay AL, Gallardo D, Rojas I, Marsh SGE, Goldman JM, Madrigal JA (1998) Mutation detection and typing of polymorphic loci through double-strand conformation analysis. Nat Genet 18(2):192–194
Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (1996–2004) Genetix 4.05., logicial sous Windows pour la génétique des populations. Laboratoire Génome, Université Montpellier, France
Bell PA, Chaturvedi S, Gelfand CA, Huang CY, Kochersperger M, Kopla R, Modica F, Pohl M, Varde S, Zhao RB, Zhao XJ, Boyce-Jacino MT (2002) SNPstream (R) UHT: ultra-high throughput SNP genotyping for pharmacogenomics and drug discovery. Biotechniques 32:70–77
Berlin S, Quintela M, Höglund J (2008) A multilocus assay reveals high nucleotide diversity and limited differentiation among Scandinavian willow grouse (Lagopus lagopus). BMC Genet 9:89
Birdlife I (2004) Birds in Europe: population estimates, trends and conservation status. Birdlife International, Cambridge
Bollmer JL, Hull JM, Ernest HB, Sarasola JH, Parker PG (2011) Reduced MHC and neutral variation in the Galapagos hawk, an island endemic. BMC Evol Biol 11:143
Both C, Artemyev AV, Blaauw B, Cowie RJ, Dekhuijzen AJ, Eeva T, Enemar A, Gustafsson L, Ivankina EV, Jarvinen A, Metcalfe NB, Nyholm NEI, Potti J, Ravussin PA, Sanz JJ, Silverin B, Slater FM, Sokolov LV, Torok J, Winkel W, Wright J, Zang H, Visser ME (2004) Large-scale geographical variation confirms that climate change causes birds to lay earlier. Proceedings of the Royal Society of London Series B-Biological Sciences 271(1549):1657–1662
Corrales C, Höglund J (2012) Maintenance of gene flow by female biased dispersal of black grouse Tetrao tetrix in northern Sweden. J. Ornithology 153:1127–1139
Corrales C, Pavlovska M, Höglund J (2014) Phylogeography and subspecies status of black grouse. J. Ornithology 155:13–25
Dyer RJ, Nason JD (2004) Population Graphs: the graph theoretic shape of genetic structure. Mol Ecol 13(7):1713–1727
Eimes JA, Bollmer JL, Whittingham LA, Johnson JA, Van Oosterhout C, Dunn PO (2011) Rapid loss of MHC class II variation in a bottlenecked population is explained by drift and loss of copy number variation. J Evol Biol 24(9):1847–1856
Ejsmond MJ, Radwan J (2011) MHC diversity in bottlenecked populations: a simulation model. Conserv Genet 12(1):129–137
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620
Excoffier L, Estoup A, Cornuet JM (2005) Bayesian analysis of an admixture model with mutations and arbitrarily linked markers. Genetics 169(3):1727–1738
Falush D, Stephens M, Pritchard J (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587
Glutz v.Blotzheim U, Bauer K, Bezzel E (1973) Handbuch der Vögel Mitteleuropas. AULA Verlag, Wiesbaden
Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered 86(6):485–486
Haig SM, Bronaugh WM, Crowhurst RS, D’Elia J, Eagles-Smith CA, Epps CW, Knaus B, Miller MP, Moses ML, Oyler-McCance S, Robinson WD, Sidlauskas B (2011) Genetic applications in avian conservation. Auk 128(2):205–229
Hoeck PEA, Bollmer JL, Parker PG, Keller LF (2011) Differentiation with drift: a spatio-temporal genetic analysis of Galapagos mockingbird populations (Mimus spp.). Philos Trans R Soc B 365(1543):1127–1138
Höglund J (2009) Evolutionary conservation genetics. Oxford University Press, Oxford
Höglund J, Larsson JK, Baines D, Corrales C, Santafe G, Segelbacher G (2011) Genetic structure among black grouse in Britain: implications for designing conservation units. Anim Conserv 14:400–408
Hubisz M, Falush D, Stephens M, Pritchard J (2009) Inferring weak population structure with the assistance of sample group information. Molecular Ecology Resources 9(5):1322–1332
Jakobsson M, Rosenberg N (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806
Johnson JA, Bellinger MR, Toepfer JE, Dunn P (2004) Temporal changes in allele frequencies and low effective population size in greater prairie-chickens. Mol Ecol 13(9):2617–2630
Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405
Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241
Kirk H, Freeland JR (2011) Applications and Implications of neutral versus non-neutral markers in molecular ecology. Int J Mol Sci 12(6):3966–3988
La Haye MJJ, Neumann K, Koelewijn HP (2012) Strong decline of gene diversity in local populations of the highly endangered Common hamster (Cricetus cricetus) in the western part of its European range. Conserv Genet 13(2):311–322
Larsson JK, Jansman HAH, Segelbacher G, Hoglund J, Koelewijn HP (2008) Genetic impoverishment of the last black grouse (Tetrao tetrix) population in the Netherlands: detectable only with a reference from the past. Mol Ecol 17(8):1897–1904
Leonard JA (2008) Ancient DNA applications for wildlife conservation. Mol Ecol 17(19):4186–4196
Ludwig GX, Alatalo RV, Helle P, Linden H, Lindstrom J, Siitari H (2006) Short- and long-term population dynamical consequences of asymmetric climate change in black grouse. Proceedings of the Royal Society B-Biological Sciences 273(1597):2009–2016
Ludwig GX, Alatalo RV, Helle P, Nissinen K, Siitari H (2008) Large-scale drainage and breeding success in boreal forest grouse. J Appl Ecol 45(1):325–333
Manel S, Berthier P, Luikart G (2002) Detecting wildlife poaching: Identifying the origin of individuals with Bayesian assignment tests and multilocus genotypes. Conserv Biol 16(3):650–659
Klaus S, Bergmann H, Marti C, Müller F, Vitovic OA, Wiesner J (1990) Die Birkhühner.—Neue Brehm-Bücherei. Ziemsen Verlag, Wittenberg Lutherstadt
Martinez-Cruz B, Godoy JA, Negro JJ (2007) Population fragmentation leads to spatial and temporal genetic structure in the endangered Spanish imperial eagle. Mol Ecol 16(3):477–486
McKelvey KS, Schwartz MK (2005) DROPOUT: a program to identify problem loci and samples for noninvasive genetic samples in a capture-mark-recapture framework. Mol Ecol Notes 5(3):716–718
Meirmans PG (2006) Using the AMOVA framework to estimate a standardized genetic differentiation measure. Evolution 60(11):2399–2402
Meirmans PG, Hedrick PW (2011) Assessing population structure: FST and related measures. Molecular Ecology Resources 11(1):5–18
Miller HC, Lambert DM (2004) Genetic drift outweighs balancing selection in shaping post-bottleneck major histocompatibility complex variation in New Zealand robins (Petroicidae). Mol Ecol 13:3709–3721
Miller HC, Allendorf F, Daugherty CH (2010) Genetic diversity and differentiation at MHC genes in island populations of tuatara (Sphenodon spp.). Mol Ecol 19(18):3894–3908
Nei M (1972) Genetic distance between populations. Am Nat 106(949):283–292
Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590
Peakall R, Smouse PE (2006) GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6(1):288–295
Piertney SB, Hoglund J (2001) Polymorphic microsatellite DNA markers in black grouse (Tetrao tetrix). Mol Ecol Notes 1(4):303–304
Piertney SB, Oliver MK (2006) The evolutionary ecology of the major histocompatibility complex. Heredity 96(1):7–21
Radwan J, Biedrzycka A, Babik W (2010) Does reduced MHC diversity decrease viability of vertebrate populations? Biol Conserv 143(3):537–544
Richardson DS, Westerdahl H (2003) MHC diversity in two Acrocephalus species: the outbred Great reed warbler and the inbred Seychelles warbler. Mol Ecol 12(12):3523–3529
Rowe KC, Singhal S, Macmanes MD, Ayroles JF, Morelli TL, Rubidge EM, Bi K, Moritz CC (2011) Museum genomics: low-cost and high-accuracy genetic data from historical specimens. Molecular Ecology Resources 11(6):1082–1092
Segelbacher G, Paxton RJ, Steinbrueck G, Trontelj P, Storch I (2000) Characterisation of microsatellites in capercaillie (Tetrao urogallus) (AVES). Mol Ecol 9:1934–1935
Segelbacher G, Manel S, Tomiuk J (2008) Temporal and spatial analyses disclose consequences of habitat fragmentation on the genetic diversity in capercaillie (Tetrao urogallus). Mol Ecol 17:2356–2367
Smulders MJM, Snoek LB, Booy G, Vosman B (2003) Complete loss of MHC genetic diversity in the Common Hamster (Cricetus cricetus) population in The Netherlands. Consequences for conservation strategies. Conserv Genet 4(4):441–451
Sommer S (2005) The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Front Zool 2:16
Strand T, Höglund J (2011) Genotyping of black grouse MHC class II B using reference Strand-Mediated Conformational Analysis (RSCA). BMC Research Notes 4(1):183
Strand AE, Niehaus JM (2007) KERNELPOP, a spatially explicit population genetic simulation engine. Mol Ecol Notes 7:969–973
Strand TM, Segelbacher G, Quintela M, Xiao L, Axelsson T, Höglund J (2012) Can balancing selection on MHC loci counteract genetic drift in small fragmented populations of black grouse? Ecology and Evolution 2:341–353
Strand T, Wang B, Meyer-Lucht Y, Höglund J (2013) Evolutionary history of black grouse major histocompatibility complex class IIB genes revealed through single locus sequence-based genotyping. BMC Genet 14:29
Sutton J, Nakagawa S, Robertson B, Jamieson IG (2011) Disentangling the roles of natural selection and genetic drift in shaping variation at MHC immunity genes. Molecular Ecoloy 20(21):4408–4420
Tracy LN, Jamieson IG (2011) Historic DNA reveals contemporary population structure results from anthropogenic effects, not pre-fragmentation patterns. Conserv Genet 12(2):517–526
Valiere N (2002) GIMLET: a computer program for analysing genetic individual identification data. Mol Ecol Notes 2(3):377–379
Van Oosterhout C (2009) A new theory of MHC evolution: beyond selection on the immune genes. Proceedings Of The Royal Society B-Biological Sciences 276(1657):657–665
Van Oosterhout CV, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538
Wandeler P, Hoeck PEA, Keller LF (2007) Back to the future: museum specimens in population genetics. Trends Ecol Evol 22(12):634–642
Wang B, Ekblom R, Strand TM, Portela-Bens S, Höglund J (2012) Sequencing of the core MHC region of black grouse (Tetrao tetrix) and comparative genomics of the galliform MHC. BMC Genom 13:553
Warren PK, Baines D (2002) Dispersal, survival and causes of mortality in black grouse Tetrao tetrix in northern England. Wildlife Biol 8(2):91–97
Weir BS, Cockerham CC (1984) Estimating F statistics for the analysis of population-structure. Evolution 38(6):1358–1370
Westerdahl H, Wittzell H, von Schantz T, Bensch S (2004) MHC class I typing in a songbird with numerous loci and high polymorphism using motif-specific PCR and DGGE. Heredity 92(6):534–542
Wübbenhorst J, Prüter J (2007) Grundlagen für ein Artenhilfsprogramm “Birkhuhn in Niedersachsen”. Naturschutz und Landschaftspflege in Niedersachsen
Acknowledgments
We are grateful to Lungyun Xiao who assisted with the laborator work. Thanks to Robin Strand for calculating MHC APD. We thank Verein Naturschutzpark Lüneburger Heide, Hunting Association Niedersachsen and Schleswig–Holstein, the Copenhagen Natural History Museum, the Museum of the University Hamburg, the Museum of Naturkunde Berlin and the Museum of Halberstadt and the Dutch Natural History Museum—Naturalis for providing samples. This work was funded through Deutsche Wildtier Stiftung (to GS) and by the Swedish Research Council (VR to JH).
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Segelbacher, G., Strand, T.M., Quintela, M. et al. Analyses of historical and current populations of black grouse in Central Europe reveal strong effects of genetic drift and loss of genetic diversity. Conserv Genet 15, 1183–1195 (2014). https://doi.org/10.1007/s10592-014-0610-3
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DOI: https://doi.org/10.1007/s10592-014-0610-3