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Characterizing range-wide divergence in an alpine-endemic bird: a comparison of genetic and genomic approaches

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Abstract

The delineation of intraspecific units that are evolutionarily and demographically distinct is an important step in the development of species-specific management plans. Neutral genetic variation has served as the primary data source for delineating “evolutionarily significant units,” but with recent advances in genomic technology, we now have an unprecedented ability to utilize information about neutral and adaptive variation across the entire genome. Here, we use traditional genetic markers (microsatellites) and a newer reduced-representation genomic approach (single nucleotide polymorphisms) to delineate distinct groups of white-tailed ptarmigan (Lagopus leucura), an alpine-obligate species that is distributed in naturally fragmented habitats from Alaska to New Mexico. Five subspecies of white-tailed ptarmigan are currently recognized but their distinctiveness has not been verified with molecular data. Based on analyses of 436 samples at 12 microsatellite loci and 95 samples at 14,866 single nucleotide polymorphism loci, we provide strong support for treating two subspecies as distinct intraspecific units—L. l. altipetens, found in Colorado and neighboring states; and L. l. saxatilis, found on British Columbia’s Vancouver Island—but our findings reveal more moderate patterns of divergence within the remainder of the species’ range. Results based on genetic and genomic datasets generally agreed with one another, indicating that in many cases microsatellite loci may be sufficient for describing major patterns of genetic structure across species’ ranges. This work will inform future conservation and management decisions for the white-tailed ptarmigan, a species that may be vulnerable to future changes in climate.

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Data availability

All datasets are available in the online supplement. In addition, the molecular datasets are archived at https://doi.org/10.5066/F7GM86GZ and the genomic sequencing data are deposited in Genbank (biosample accession numbers: SAMN08132751-SAMN08132845).

References

  • Aldrich JW (1963) Geographic orientation of American Tetraonidae. J Wildl Manag 27:529–545

    Article  Google Scholar 

  • Allendorf FW, Luikart GH (2007) Conservation and the genetics of populations. Wiley, Hoboken

    Google Scholar 

  • Allendorf FW, Hohenlohe PA, Luikart G (2010) Genomics and the future of conservation genetics. Nature 11:697–709

    CAS  Google Scholar 

  • Altschul SF, Gish W, Miller W et al (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Avise JC, Arnold J, Ball RM et al (2008) Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annu Rev Ecol Syst 18:489–522

    Article  Google Scholar 

  • Bergmann C (1847) Ueber die Verhältnisse der Wärmeökonomie der Thiere zu ihrer Grösse. Gottinger Stud 3:595–708

    Google Scholar 

  • Bi K, Linderoth T, Vanderpool D et al (2013) Unlocking the vault: next-generation museum population genomics. Mol Ecol 22:6018–6032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blackburn TM, Gaston KJ, Loder N, Jul N (1999) Geographic gradients in body size: a clarification of Bergmann’ s rule. Divers Distrib 5:165–174

    Article  Google Scholar 

  • Bradbury IR, Hubert S, Higgins B et al (2013) Genomic islands of divergence and their consequences for the resolution of spatial structure in an exploited marine fish. Evol Appl 6:450–461

    Article  PubMed  PubMed Central  Google Scholar 

  • Braun CE, Williams SO (2015) History and status of the white-tailed ptarmigan in New Mexico. West Birds 46:233–243

    Google Scholar 

  • Braun CE, Hoffman RW, Rogers GE (1976) Wintering areas and winter ecology of white-tailed ptarmigan in Colorado. Special report (Division of Wildlife, Colorado); No. 38

  • Braun CE, Nish DH, Giesen KM (1978) Release and establishment of white-tailed ptarmigan in Utah. Southwest Nat 23:661–667

    Article  Google Scholar 

  • Braun CE, Taylor WP, Ebbert SE et al (2011) Protocols for successful translocation of ptarmigan. Gyrfalcons Ptarmigan Chang World 2:339–348

    Google Scholar 

  • Camacho C, Coulouris G, Avagyan V et al (2009) BLAST plus: architecture and applications. BMC Bioinform 10:1

    Article  Google Scholar 

  • Chapman FM (1902) List of birds collected in Alaska by the Andrew J. Stone Expedition of 1901. Bull Am Mus Nat Hist 16:231

    Google Scholar 

  • Clements JF, Schulenberg TS, Iliff MJ et al (2018) The eBird/Clements checklist of birds of the world: v2016. http://www.birds.cornell.edu/clementschecklist/download/

  • Crandall K, Bininda-Emonds O, Mace G, Wayne R (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295

    Article  CAS  PubMed  Google Scholar 

  • Dickinson EC, Remsen JJV (2013) The Howard and Moore complete checklist of the birds of the world, 4th edn, vol 1. Non-passerines

  • Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Fedy BC, Martin K, Ritland C, Young J (2008) Genetic and ecological data provide incongruent interpretations of population structure and dispersal in naturally subdivided populations of white-tailed ptarmigan (Lagopus leucura). Mol Ecol 17:1905–1917

    Article  CAS  PubMed  Google Scholar 

  • Fike JA, Oyler-McCance SJ, Zimmerman SJ, Castoe TA (2015) Development of 13 microsatellites for Gunnison Sage-grouse (Centrocercus minimus) using next-generation shotgun sequencing and their utility in Greater Sage-grouse (Centrocercus urophasianus). Conserv Genet Resour 7:211–214

    Article  Google Scholar 

  • Frankham R, Ballou JD, Eldridge MDB et al (2011) Predicting the probability of outbreeding depression. Conserv Biol 25:465–475

    Article  PubMed  Google Scholar 

  • Frantz AC, Cellina S, Krier A et al (2009) Using spatial Bayesian methods to determine the genetic structure of a continuously distributed population: clusters or isolation by distance? J Appl Ecol 46:493–505

    Article  Google Scholar 

  • Fraser D, Bernatchez L (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Mol Ecol 10:2741–2752

    Article  CAS  PubMed  Google Scholar 

  • Funk WC, McKay JK, Hohenlohe PA, Allendorf FW (2012) Harnessing genomics for delineating conservation units. Trends Ecol Evol 27:489–496

    Article  PubMed  PubMed Central  Google Scholar 

  • Gautier M (2015) Genome-wide scan for adaptive divergence and association with population-specific covariates. Genetics 201:1555–1579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giesen KM, Braun CE (1993) Natal dispersal and recruitment of juvenile white-tailed ptarmigan in Colorado. J Wildl Manag 57:72–77

    Article  Google Scholar 

  • Gill F, Donsker D (eds) (2018) IOC World Bird List (v 8.2). https://doi.org/10.14344/IOC.ML.8.2

  • Günther T, Coop G (2013) Robust identification of local adaptation from allele frequencies. Genetics 195:205–220

    Article  PubMed  PubMed Central  Google Scholar 

  • Hoffman RW (2006) White-tailed ptarmigan (Lagopus leucura): a technical conservation assessment. Report prepared for the USDA Forest Service, Rocky Mountain Region, Species Conservation Project. p 72

  • Hoffman RW, Giesen KM (1983) Demography of an introduced population of white-tailed ptarmigan. Can J Zool 61:1758–1764

    Article  Google Scholar 

  • Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70

    Google Scholar 

  • Holycross AT, Douglas ME (2007) Geographic isolation, genetic divergence, and ecological non-exchangeability define ESUs in a threatened sky-island rattlesnake. Biol Conserv 134:142–154

    Article  Google Scholar 

  • Jackson MM, Gergel SE, Martin K (2015) Effects of climate change on habitat availability and configuration for an endemic coastal alpine bird. PLoS ONE 10:e0142110

    Article  PubMed  PubMed Central  Google Scholar 

  • Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806

    Article  CAS  PubMed  Google Scholar 

  • Jombart T (2008) adegenet: A R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405

    CAS  PubMed  Google Scholar 

  • Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94

    Article  PubMed  PubMed Central  Google Scholar 

  • Jones OR, Wang J (2010) COLONY: a program for parentage and sibship inference from multilocus genotype data. Mol Ecol Resour 10:551–555

    Article  PubMed  Google Scholar 

  • Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026

    Article  PubMed  Google Scholar 

  • Kanthaswamy S, Kurushima JD, Smith DG (2006) Inferring Pongo conservation units: a perspective based on microsatellite and mitochondrial DNA analyses. Primates 47:310–321

    Article  PubMed  Google Scholar 

  • Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241

    Article  Google Scholar 

  • Kivioja T, Vähärautio A, Karlsson K et al (2011) Counting absolute numbers of molecules using unique molecular identifiers. Nat Methods 9:72–74

    Article  PubMed  Google Scholar 

  • Kopelman NM, Mayzel J, Jakobsson M et al (2015) Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour 15:1179–1191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Langmead B, Salzberg SL (2013) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359

    Article  Google Scholar 

  • Li W, Godzik A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22:1658–1659

    Article  CAS  PubMed  Google Scholar 

  • Li H, Handsaker B, Wysoker A et al (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25:2078–2079

    Article  PubMed  PubMed Central  Google Scholar 

  • Manel S, Schwartz MK, Luikart G, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics. Trends Ecol Evol 18:189–197

    Article  Google Scholar 

  • Martin K (2001) Wildlife in alpine and sub-alpine habitats. In: Johnson DH, O’Neil TA (eds) Wildlife-habitat relationships in Oregon and Washington. Oregon State University Press, Corvallis, pp 285–310

    Google Scholar 

  • Martin K, Brown GA, Young JR (2004) The historic and current distribution of the Vancouver Island White-tailed Ptarmigan (Lagopus leucurus saxatilis). J Field Ornithol 75:239–256

    Article  Google Scholar 

  • Martin K, Robb LA, Wilson S, Braun CE (2015) White-tailed Ptarmigan (Lagopus leucura). In: Rodewald PG (ed) The birds of North America. Cornell Lab of Ornithology, Ithaca; Retrieved from the Birds of North America: https://birdsna.org/Species-Account/bna/species/whtpta1

  • McTaggart Cowan I (1938) The white-tailed ptarmigan of Vancouver Island. Condor 41:82–83

    Google Scholar 

  • Moritz C (1994) Defining “evolutionarily significant units” for conservation. Trends Ecol Evol 9:373–375

    Article  CAS  PubMed  Google Scholar 

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nei M, Genetics P (1973) Analysis of gene diversity in subdivided populations. Proc Nat Acad Sci USA 70:3321–3323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York

    Google Scholar 

  • Osgood WH (1901) New subspecies of North American birds. Auk 18:179–185

    Article  Google Scholar 

  • Oyler-McCance SJ, Oh KP, Langin KM, Aldridge CL (2016) A field ornithologist’s guide to genomics: Practical considerations for ecology and conservation. Auk Ornithol Adv 133:626–648

    Google Scholar 

  • Prince DJ, O’Rourke SM, Thompson TQ et al (2017) The evolutionary basis of premature migration in Pacific salmon highlights the utility of genomics for informing conservation. Sci Adv 3:e1603198

    Article  PubMed  PubMed Central  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Puechmaille SJ (2016) The program structure does not reliably recover the correct population structure when sampling is uneven: subsampling and new estimators alleviate the problem. Mol Ecol Resour 16:608–627

    Article  PubMed  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (Version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Article  Google Scholar 

  • Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138

    Article  Google Scholar 

  • Ryder OA (1986) Species conservation and systematics: the dilemma of subspecies. Trends Ecol Evol 1:9–10

    Article  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Schwartz MK, McKelvey KS (2009) Why sampling scheme matters: The effect of sampling scheme on landscape genetic results. Conserv Genet 10:441–452

    Article  Google Scholar 

  • Segelbacher G, Paxton R, Steinbruck G et al (2000) Characterization of microsatellites in capercaillie Tetrao urogallus (AVES). Mol Ecol 9:1934–1935

    Article  CAS  PubMed  Google Scholar 

  • Segelbacher G, Cushman SA, Epperson BK et al (2010) Applications of landscape genetics in conservation biology: concepts and challenges. Conserv Genet 11:375–385

    Article  Google Scholar 

  • Seglund AE (2012) White-tailed ptarmigan summary report 2011 and project proposal 2012. Colorado Parks and Wildlife

  • Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236:787–792

    Article  CAS  PubMed  Google Scholar 

  • Taylor WP (1920) A new ptarmigan from Mount Rainier. Condor 22:146–152

    Article  Google Scholar 

  • Toews DPL, Campagna L, Taylor SA et al (2016) Genomic approaches to understanding the early stages of population divergence and speciation in birds. Auk 133:13–30

    Article  Google Scholar 

  • USFWS NMFS (1996) Policy regarding recognition of distinct vertebrate population segments under the Endangered Species Act. Fed Regist 61:4721–4725

    Google Scholar 

  • USFWS (2012) Endangered and threatened wildlife and plants; 90-day finding on a petition to list the southern White-Tailed Ptarmigan and the Mt. Rainier White-Tailed Ptarmigan as Threatened With Critical Habitat. Fed Regist 77:33143–33155

    Google Scholar 

  • Van Oosterhout C, 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

    Article  Google Scholar 

  • Wann GT, Aldridge CL, Braun CE (2014) Estimates of annual survival, growth, and recruitment of a white-tailed ptarmigan population in Colorado over 43 years. Popul Ecol 56:555–567

    Article  Google Scholar 

  • Waples RS (1991) Pacific salmon, Oncorynchus spp., and the definition of “species” under the Endangered Species Act. Mar Fish Rev 53:11–22

    Google Scholar 

  • Waples R (1995) Evolutionarily significant units and the conservation of biological diversity under the Endangered Species Act. Am Fish Soc Symp 8–27

  • Waples RS, Anderson EC (2017) Purging putative siblings from population genetic datasets: a cautionary view. Mol Ecol 26:1211–1224

    Article  PubMed  Google Scholar 

  • West-Eberhard MJ (1989) Phenotypic plasticity and the origins of diversity. Annu Rev Ecol Syst 20:249–278

    Article  Google Scholar 

  • Wilson A, Bonaparte CL (1831) American ornithology, vol 4 (Jameson R (ed)). Constable, Edinburgh

    Google Scholar 

  • Wilson S, Martin K (2011) Life-history and demographic variation in an alpine specialist at the latitudinal extremes of the range. Popul Ecol 53:459–471

    Article  Google Scholar 

  • Winter DJ (2012) MMOD: An R library for the calculation of population differentiation statistics. Mol Ecol Resour 12:1158–1160

    Article  CAS  PubMed  Google Scholar 

  • Zwickel F, Bendell J (1967) A snare for capturing blue grouse. J Wildl Manag 31:202–204

    Article  Google Scholar 

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Acknowledgements

We thank Kathryn Bernier, Sharon Birks, John Bulger, Ray Collingwood, Avery Cook, Sarah Hudson, Doug Jury, Lee Kaiser, Richard Merizon, Jason Robinson, Serena Rocksund, William Taylor, and many others for help obtaining ptarmigan samples. We also thank Daniel Taylor for digitizing the morphology data, Kevin Oh for advice on genomic methods, and Christin Pruett and Patricia Stevens for manuscript comments. The University of Washington Burke Museum provided four samples through their tissue collection program. Colorado Parks and Wildlife, the Utah Division of Wildlife Resources, and the Alaska Department of Fish and Game provided samples collected by hunters. Funding was provided by the U.S. Geological Survey, the U.S. National Park Service, the Natural Sciences and Engineering Research Council of Canada, Forest Renewal British Columbia, Environment and Climate Change Canada, Colorado Parks and Wildlife, the Washington Department of Fish and Wildlife, and the Utah Division of Wildlife Resources. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

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Authors and Affiliations

  1. Fort Collins Science Center, U.S. Geological Survey, Fort Collins, CO, USA

    Kathryn M. Langin, Jennifer A. Fike, R. Scott Cornman & Sara J. Oyler-McCance

  2. Natural Resource Ecology Laboratory, Department of Ecosystem Science and Sustainability, In Cooperation with the U.S. Geological Survey, Colorado State University, Fort Collins, CO, USA

    Cameron L. Aldridge & Gregory T. Wann

  3. Department of Forest and Conservation Sciences, University of British Columbia, Vancouver, BC, Canada

    Kathy Martin

  4. Wildlife Research Division, Environment and Climate Change Canada, Delta, BC, Canada

    Kathy Martin

  5. Colorado Parks and Wildlife, Montrose, CO, USA

    Amy E. Seglund

  6. Washington Department of Fish and Wildlife, P.O. Box 1077, Bridgeport, WA, USA

    Michael A. Schroeder

  7. Grouse Inc., 5572 North Ventana Vista Road, Tucson, USA

    Clait E. Braun

  8. Department of Biology, Marian University, Indianapolis, IN, USA

    David P. Benson

  9. School of Environment, Resources and Sustainability, University of Waterloo, Waterloo, ON, Canada

    Brad C. Fedy

  10. Environment and Sustainability Department, Western State Colorado University, Gunnison, CO, USA

    Jessica R. Young

  11. Wildlife Research Division, National Wildlife Research Centre, Environment and Climate Change Canada, Ottawa, ON, Canada

    Scott Wilson

  12. G. M. Sutton Avian Research Center, P.O. Box 2007, Bartlesville, OK, USA

    Donald H. Wolfe

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  1. Kathryn M. Langin
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  2. Cameron L. Aldridge
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Correspondence to Kathryn M. Langin.

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Langin, K.M., Aldridge, C.L., Fike, J.A. et al. Characterizing range-wide divergence in an alpine-endemic bird: a comparison of genetic and genomic approaches. Conserv Genet 19, 1471–1485 (2018). https://doi.org/10.1007/s10592-018-1115-2

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