Genetic depletion at adaptive but not neutral loci in an endangered bird species

Molecular Ecology

Volumn 23, Issue 23, 2014, Pages 5712-5725

  Hartmann, Stefanie A ^a   Schaefer, H Martin ^a   Segelbacher, Gernot ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Atlapetes pallidiceps; bottleneck; conservation genetics; genetic diversity; microsatellites; Toll like receptors

Indexed keywords

ATLAPETES PALLIDICEPS; AVES;

MICROSATELLITE DNA; TOLL LIKE RECEPTOR;

ADAPTATION; ANIMAL; BIOLOGICAL MODEL; DNA SEQUENCE; ECUADOR; ENDANGERED SPECIES; ENVIRONMENTAL PROTECTION; FINCH; GENE LOCUS; GENETIC VARIABILITY; GENETICS; POPULATION GENETICS;

ADAPTATION, BIOLOGICAL; ANIMALS; CONSERVATION OF NATURAL RESOURCES; ECUADOR; ENDANGERED SPECIES; FINCHES; GENETIC LOCI; GENETIC VARIATION; GENETICS, POPULATION; MICROSATELLITE REPEATS; MODELS, GENETIC; SEQUENCE ANALYSIS, DNA; TOLL-LIKE RECEPTORS;

EID: 84912123134     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.12975     Document Type: Article

References (75)

1. Agreda A, Krabbe N, Rodriguez O, (1999) Pale Headed Brushfinch Atlapetes pallidiceps is not extinct. Cotinga, 11, 50-54.
2. Agudo R, Alcaide M, Rico C, et al,. (2011) Major histocompatibility complex variation in insular populations of the Egyptian vulture: inferences about the roles of genetic drift and selection. Molecular Ecology, 20, 2329-2340.
3. Aguilar A, Roemer G, Debenham S, et al,. (2004) High MHC diversity maintained by balancing selection in an otherwise genetically monomorphic mammal. Proceedings of the National Academy of Sciences of the United States of America, 101, 3490-3494.
4. Alcaide M, Edwards SV, (2011) Molecular evolution of the toll-like receptor multigene family in birds. Molecular Biology and Evolution, 28, 1703-1715.
5. Alho JS, Valimaki K, Merila J, (2010) rhh: an R extension for estimating multilocus heterozygosity and heterozygosity-heterozygosity correlation. Molecular Ecology Resources, 10, 720-722.
6. Ardern SL, Lambert DM, (1997) Is the black robin in genetic peril? Molecular Ecology, 6, 21-28.
7. Babik W, (2010) Methods for MHC genotyping in non-model vertebrates. Molecular Ecology Resources, 10, 237-251.
8. Babik W, Pabijan M, Arntzen JW, et al,. (2009) Long-term survival of a urodele amphibian despite depleted major histocompatibility complex variation. Molecular Ecology, 18, 769-781.
9. Barrett RDH, Schluter D, (2008) Adaptation from standing genetic variation. Trends in Ecology & Evolution, 23, 38-44.
10. BirdLife (2013) BirdLife's online World Bird Database. In. BirdLife International. Available from http://www.birdlife.org, Cambridge, UK.
11. Borg AA, Pedersen SA, Jensen H, Westerdahl H, (2011) Variation in MHC genotypes in two populations of house sparrow (Passer domesticus) with different population histories. Ecology and evolution, 1, 145-159.
12. Bouzat JL, Cheng HH, Lewin HA, et al,. (1998) Genetic evaluation of a demographic bottleneck in the Greater Prairie Chicken. Conservation Biology, 12, 836-843.
13. Brooks SP, Gelman A, (1998) General methods for monitoring convergence of iterative simulations. Journal of Computational and Graphical Statistics, 7, 434-455.
14. de Bruyn M, Pinsky ML, Hall B, et al,. (2014) Rapid increase in southern elephant seal genetic diversity after a founder event. Proceedings of the Royal Society B-Biological Sciences, 281, 20133078.
15. Busch JD, Waser PM, DeWoody JA, (2007) Recent demographic bottlenecks are not accompanied by a genetic signature in banner-tailed kangaroo rats (Dipodomys spectabilis). Molecular Ecology, 16, 2450-2462.
16. Butchart SHM, Stattersfield AJ, Collar NJ, (2006) How many bird extinctions have we prevented? Oryx, 40, 266-278.
17. Cornuet JM, Luikart G, (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics, 144, 2001-2014.
18. Darvill B, Ellis JS, Lye GC, Goulson D, (2006) Population structure and inbreeding in a rare and declining bumblebee, Bombus muscorum (Hymenoptera: Apidae). Molecular Ecology, 15, 601-611.
19. Dercon G, Bossuyt B, Bievre BD, Cisneros F, Deckers J, (1998) Zonaficacion agroecologica del Austro Ecuatoriano. Universidad de Cuenca, Ecuador.
20. Earl DA, Vonholdt BM, (2012) structure harvester: a website and program for visualizing structure output and implementing the Evanno method. Conservation Genetics Resources, 4, 359-361.
21. Ellegren H, Hartman G, Johansson M, Andersson L, (1993) Major histocompatibility complex monomorphism and low-levels of DNA-fingerprinting variability in a reintroduced and rapidly expanding population of beavers. Proceedings of the National Academy of Sciences of the United States of America, 90, 8150-8153.
22. Evanno G, Regnaut S, Goudet J, (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Molecular Ecology, 14, 2611-2620.
23. Evett I, Weir B, (1998) Interpreting DNA evidence: Statistical Genetics for Forensic Scientists. Sinauer Associates, Sunderland.
24. Forstmeier W, Schielzeth H, Mueller JC, Ellegren H, Kempenaers B, (2012) Heterozygosity-fitness correlations in zebra finches: microsatellite markers can be better than their reputation. Molecular Ecology, 21, 3237-3249.
25. Frankham R, (2005) Genetics and extinction. Biological Conservation, 126, 131-140.
26. Garcia-Moreno J, Fjeldsa J, (1999) Re-evaluation of species limits in the genus Atlapetes based on mtDNA sequence data. Ibis, 141, 199-207.
27. Goossens B, Chikhi L, Ancrenaz M, et al,. (2006) Genetic signature of anthropogenic population collapse in orang-utans. Plos Biology, 4, 285-291.
28. Goudet J, (1995) fstat (Version 1.2): a computer program to calculate F-statistics. Journal of Heredity, 86, 485-486.
29. Greenwald KR, (2010) Genetic data in population viability analysis: case studies with ambystomatid salamanders. Animal Conservation, 13, 115-122.
30. Groombridge JJ, Jones CG, Bruford MW, Nichols RA, (2000) Conservation biology-'Ghost' alleles of the Mauritius kestrel. Nature, 403, 616.
31. Grueber CE, Jamieson IG, (2013) Primers for amplification of innate immunity toll-like receptor loci in threatened birds of the Apterygiformes, Gruiformes, Psittaciformes and Passeriformes. Conservation Genetics Resources, 5, 1043-1047.
32. Grueber CE, Wallis GP, King TM, Jamieson IG, (2012) Variation at innate immunity toll-like receptor genes in a Bottlenecked Population of a New Zealand Robin. PLoS ONE, 7, e45011.
33. Hall TA, (1999) bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95-98.
34. Hartmann SA, Schaefer HM, Segelbacher G, (2014) Development of 12 microsatellite loci for the endangered Pale-headed Brushfinch (Atlapetes pallidiceps) and their cross-Amplification in two co-occurring Brushfinches. Journal of Ornithology, 155, 835-839.
35. Iwasaki A, Medzhitov R, (2010) Regulation of adaptive immunity by the innate immune system. Science, 327, 291-295.
36. 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.
37. Jansson E, Ruokonen M, Kojola I, Aspi J, (2012) Rise and fall of a wolf population: genetic diversity and structure during recovery, rapid expansion and drastic decline. Molecular Ecology, 21, 5178-5193.
38. Jarne P, Lagoda PJL, (1996) Microsatellites, from molecules to populations and back. Trends in Ecology & Evolution, 11, 424-429.
39. Jombart T, (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics, 24, 1403-1405.
40. Kalinowski ST, Taper ML, Marshall TC, (2007) Revising how the computer program cervus accommodates genotyping error increases success in paternity assignment. Molecular Ecology, 16, 1099-1106.
41. Kirk H, Freeland JR, (2011) Applications and implications of neutral versus non-neutral markers in molecular ecology. International Journal of Molecular Sciences, 12, 3966-3988.
42. Krabbe N, Juina M, Sornoza AF, (2011) Marked population increase in Pale-headed Brush-finch Atlapetes pallidiceps in response to cowbird control. Journal of Ornithology, 152, 219-222.
43. Kvist L, Giralt D, Valera F, et al,. (2011) Population decline is accompanied by loss of genetic diversity in the Lesser Grey Shrike Lanius minor. Ibis, 153, 98-109.
44. Lande R, (1998) Risk of population extinction from fixation of deleterious and reverse mutations. Genetica, 102-3, 21-27.
45. Librado P, Rozas J, (2009) Dnasp v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451-1452.
46. Luikart G, Allendorf FW, Cornuet JM, Sherwin WB, (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. Journal of Heredity, 89, 238-247.
47. Madsen T, Stille B, Shine R, (1996) Inbreeding depression in an isolated population of adders Vipera berus. Biological Conservation, 75, 113-118.
48. Miller HC, Lambert DM, (2004) Genetic drift outweighs balancing selection in shaping post-bottleneck major histocompatibility complex variation in New Zealand robins (Petroicidae). Molecular Ecology, 13, 3709-3721.
49. Miller HC, Miller KA, Daugherty CH, (2008) Reduced MHC variation in a threatened tuatara species. Animal Conservation, 11, 206-214.
50. Mills LS, Citta JJ, Lair KP, Schwartz MK, Tallmon DA, (2000) Estimating animal abundance using noninvasive DNA sampling: promise and pitfalls. Ecological Applications, 10, 283-294.
51. Niskanen AK, Kennedy LJ, Ruokonen M, et al,. (2014) Balancing selection and heterozygote advantage in major histocompatibility complex loci of the bottlenecked Finnish wolf population. Molecular Ecology, 23, 875-889.
52. O'Grady JJ, Brook BW, Reed DH, et al,. (2006) Realistic levels of inbreeding depression strongly affect extinction risk in wild populations. Biological Conservation, 133, 42-51.
53. Oppel S, Schaefer HM, Schmidt V, Schroder B, (2004) Habitat selection by the pale-headed brush-finch (Atlapetes pallidiceps) in southern Ecuador: implications for conservation. Biological Conservation, 118, 33-40.
54. Peakall R, Smouse PE, (2006) genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes, 6, 288-295.
55. Pickles RSA, Groombridge JJ, Rojas VDZ, et al,. (2012) Genetic diversity and population structure in the endangered giant otter, Pteronura brasiliensis. Conservation Genetics, 13, 235-245.
56. Pritchard JK, Stephensa M, Donnellya P, (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945-959.
57. Pritchard JK, Pickrell JK, Coop G, (2010) The genetics of human adaptation: hard sweeps, soft sweeps, and polygenic adaptation. Current Biology, 20, R208-R215.
58. Reed DH, Frankham R, (2003) Correlation between fitness and genetic diversity. Conservation Biology, 17, 230-237.
59. Richardson DS, Westerdahl H, (2003) MHC diversity in two Acrocephalus species: the outbred Great reed warbler and the inbred Seychelles warbler. Molecular Ecology, 12, 3523-3529.
60. Rosenberg NA, (2004) distruct: a program for the graphical display of population structure. Molecular Ecology Notes, 4, 137-138.
61. Rousset F, (2008) genepop 07: a complete re-implementation of the genepop software for Windows and Linux. Molecular Ecology Resources, 8, 103-106.
62. Simonsen KL, Churchill GA, Aquadro CF, (1995) Properties of statistical tests of neutrality for DNA polymorphism data. Genetics, 141, 413-429.
63. Stephens M, Donnelly P, (2003) A comparison of Bayesian methods for haplotype reconstruction from population genotype data. American Journal of Human Genetics, 73, 1162-1169.
64. Storz JF, Beaumont MA, (2002) Testing for genetic evidence of population expansion and contraction: an empirical analysis of microsatellite DNA variation using a hierarchical Bayesian model. Evolution, 56, 154-166.
65. Taylor SS, Jenkins DA, Arcese P, (2012) Loss of Mhc and neutral variation in Peary Caribou: genetic drift is not mitigated by balancing selection or exacerbated by Mhc allele distributions. PLoS ONE, 7, e36748.
66. Therneau T, (2014) A Package for Survival Analysis in S. R package version 2.37-7, Available from http://CRAN.R-project.org/package=survival.
67. Thrimawithana AH, Ortiz-Catedral L, Rodrigo A, Hauber ME, (2013) Reduced total genetic diversity following translocations? A metapopulation approach. Conservation Genetics, 14, 1043-1055.
68. Townsend SM, Jamieson IG, (2013) Molecular and pedigree measures of relatedness provide similar estimates of inbreeding depression in a bottlenecked population. Journal of Evolutionary Biology, 26, 889-899.
69. Vali U, Einarsson A, Waits L, Ellegren H, (2008) To what extent do microsatellite markers reflect genome-wide genetic diversity in natural populations? Molecular Ecology, 17, 3808-3817.
70. Vidovic D, Matzinger P, (1988) Unresponsiveness to a foreign antigen can be caused by self-tolerance. Nature, 336, 222-225.
71. Villasenor-Cardoso MI, Ortega E, (2011) Polymorphisms of innate immunity receptors in infection by parasites. Parasite Immunology, 33, 643-653.
72. Waits LP, Paetkau D, (2005) Noninvasive genetic sampling tools for wildlife biologists: a review of applications and recommendations for accurate data collection. Journal of Wildlife Management, 69, 1419-1433.
73. Wang SP, Zhu W, Gao X, et al,. (2014) Population size and time since island isolation determine genetic diversity loss in insular frog populations. Molecular Ecology, 23, 637-648.
74. Westemeier RL, Brawn JD, Simpson SA, et al,. (1998) Tracking the long-term decline and recovery of an isolated population. Science, 282, 1695-1698.
75. Willi Y, Van Buskirk J, Hoffmann AA, (2006) Limits to the adaptive potential of small populations. Annual Review of Ecology Evolution and Systematics, 37, 433-458.