in

Habitat fragmentation differentially shapes neutral and immune gene variation in a tropical bird species

  • Acevedo-Whitehouse K, Cunningham AA (2006) Is MHC enough for understanding wildlife immunogenetics? Trends Ecol Evolution 21:433–438

    Google Scholar 

  • Adriaensen F, Chardon JP, De Blust G, Swinnen E, Villalba S, Gulinck H et al. (2003) The application of ‘least-cost’ modelling as a functional landscape model. Landsc Urban Plan 64:233–247

    Google Scholar 

  • Aguilar R, Quesada M, Ashworth L, Herrerias‐Diego Y, Lobo J (2008) Genetic consequences of habitat fragmentation in plant populations: susceptible signals in plant traits and methodological approaches. Mol Ecol 17:5177–5188

    PubMed  Google Scholar 

  • Alcaide M, Edwards SV (2011) Molecular evolution of the toll-like receptor multigene family in birds. Mol Biol Evolution 28:1703–1715

    CAS  Google Scholar 

  • Allendorf FW, Luikart G, Aitken SN (2013) Conservation and the genetics of populations, second edn. Wiley-Blackwell, Chichester, West Sussex

    Google Scholar 

  • Altizer S, Harvell D, Friedle E (2003) Rapid evolutionary dynamics and disease threats to biodiversity. Trends Ecol Evolution 18:589–596

    Google Scholar 

  • Areal H, Abrantes J, Esteves PJ (2011) Signatures of positive selection in toll-like receptor (TLR) genes in mammals. BMC Evolut Biol 11:368

    CAS  Google Scholar 

  • Arnoux E, Eraud C, Navarro N, Tougard C, Thomas A, Cavallo F et al. (2014) Morphology and genetics reveal an intriguing pattern of differentiation at a very small geographic scale in a bird species, the forest thrush Turdus lherminieri. Heredity 113:514–525

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bateson ZW, Whittingham LA, Johnson JA, Dunn PO (2015) Contrasting patterns of selection and drift between two categories of immune genes in prairie-chickens. Mol Ecol 24:6095–6106

    CAS  PubMed  Google Scholar 

  • Becker DJ, Albery GF, Kessler MK, Lunn TJ, Falvo CA, Czirják GÁ et al. (2020) Macroimmunology: the drivers and consequences of spatial patterns in wildlife immune defence. J Anim Ecol 89:972–995

    PubMed  Google Scholar 

  • Belasen AM, Bletz MC, Leite D, da S, Toledo LF, James TY (2019) Long-term habitat fragmentation is associated with reduced MHC IIB diversity and increased infections in amphibian hosts. Front Ecol Evol 6:236

    Google Scholar 

  • Bernatchez L, Landry C (2003) MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years? J Evolut Biol 16:363–377

    CAS  Google Scholar 

  • Bertrand JAM, Bourgeois YXC, Delahaie B, Duval T, García-Jiménez R, Cornuault J et al. (2014) Extremely reduced dispersal and gene flow in an island bird. Heredity 112:190–196

    CAS  PubMed  Google Scholar 

  • Biedrzycka A, Radwan J (2008) Population fragmentation and major histocompatibility complex variation in the spotted suslik, Spermophilus suslicus. Mol Ecol 17:4801–4811

    CAS  PubMed  Google Scholar 

  • Binetruy F, Buysse M, Barosi R, Duron O (2020a) Novel Rickettsia genotypes in ticks in French Guiana, South America. Sci Rep 10:1–11

    Google Scholar 

  • Binetruy F, Chevillon C, de Thoisy B, Garnier S, Duron O (2019) Survey of ticks in French Guiana. Ticks Tick Borne Dis 10:77–85

    PubMed  Google Scholar 

  • Binetruy F, Garnier S, Boulanger N, Talagrand-Reboul É, Loire E, Faivre B et al. (2020b) A novel Borrelia species, intermediate between Lyme disease and relapsing fever groups, in neotropical passerine-associated ticks. Sci Rep. 10:10596

    CAS  PubMed  PubMed Central  Google Scholar 

  • Blake JG, Loiselle BA (2012) Temporal and spatial patterns in abundance of the wedge-billed woodcreeper (Glyphorynchus spirurus) in Lowland Ecuador. Wilson J Ornithol 124:436–445

    Google Scholar 

  • Bollmer JL, Dunn PO, Whittingham LA, Wimpee C (2010) Extensive MHC class II B gene duplication in a passerine, the common yellowthroat (Geothlypis trichas). J Hered 101:448–460

    CAS  PubMed  Google Scholar 

  • Bollmer JL, Ruder EA, Johnson JA, Eimes JA, Dunn PO (2011) Drift and selection influence geographic variation at immune loci of prairie-chickens. Mol Ecol 20:4695–4706

    PubMed  Google Scholar 

  • Breitbart M, Rohwer F (2005) Here a virus, there a virus, everywhere the same virus? Trends Microbiol 13:278–284

    CAS  PubMed  Google Scholar 

  • Brown LM, Ramey RR, Tamburini B, Gavin TA (2004) Population structure and mitochondrial DNA variation in sedentary Neotropical birds isolated by forest fragmentation. Conserv Genet 5:743–757

    CAS  Google Scholar 

  • Calmont A (2012) La forêt guyanaise, entre valorisation et protection des ressources écosystémiques. VertigO – la revue électronique en sciences de l’environnement. Hors-série 14. http://journals.openedition.org/vertigo/12402

  • Cavaillon J-M (2017) Pathogen-associated molecular patterns. In: Inflammation: from molecular and cellular mechanisms to the clinic. Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim, p 17–56

  • Collinge SK (2009) Ecology of fragmented landscapes. JHU Press, Baltimore

  • Colwell DD, Dantas-Torres F, Otranto D (2011) Vector-borne parasitic zoonoses: emerging scenarios and new perspectives. Vet Parasitol 182:14–21

    PubMed  Google Scholar 

  • Cormican P, Lloyd AT, Downing T, Connell SJ, Bradley D, O’Farrelly C (2009) The avian toll-Like receptor pathway-subtle differences amidst general conformity. Dev Comp Immunol 33:967–973

    CAS  PubMed  Google Scholar 

  • Daszak P (2000) Emerging infectious diseases of wildlife—threats to biodiversity and human health. Science 287:443–449

    CAS  PubMed  Google Scholar 

  • Dawson DA, Ball AD, Spurgin LG, Martín-Gálvez D, Stewart IRK, Horsburgh GJ et al. (2013) High-utility conserved avian microsatellite markers enable parentage and population studies across a wide range of species. BMC Genomics 14:176

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dawson DA, Horsburgh GJ, Küpper C, Stewart IRK, Ball AD, Durrant KL et al. (2010) New methods to identify conserved microsatellite loci and develop primer sets of high cross-species utility—as demonstrated for birds. Mol Ecol Resour 10:475–494

    CAS  PubMed  Google Scholar 

  • DIREN Guyane (2007) Atlas des paysages de Guyane. DIREN Guyane, Cayenne

  • Dirzo R, Young HS, Galetti M, Ceballos G, Isaac NJB, Collen B (2014) Defaunation in the Anthropocene. Science 345:401–406

    CAS  PubMed  Google Scholar 

  • Downing T, Lloyd AT, O’Farrelly C, Bradley DG (2010) The differential evolutionary dynamics of avian cytokine and TLR gene classes. J Immunol 184:6993–7000

    CAS  PubMed  Google Scholar 

  • Driscoll DA, Weir T (2005) Beetle responses to habitat fragmentation depend on ecological traits, habitat condition, and remnant size. Conserv Biol 19:182–194

    Google Scholar 

  • Eckert CG, Samis KE, Lougheed SC (2008) Genetic variation across species’ geographical ranges: the central–marginal hypothesis and beyond. Mol Ecol 17:1170–1188

    CAS  Google Scholar 

  • Eizaguirre C, Lenz TL, Kalbe M, Milinski M (2012) Rapid and adaptive evolution of MHC genes under parasite selection in experimental vertebrate populations. Nat Commun 3:1–6

    Google Scholar 

  • Evans ML, Neff BD, Heath DD (2010) MHC genetic structure and divergence across populations of Chinook salmon (Oncorhynchus tshawytscha). Heredity 104:449–459

    CAS  PubMed  Google Scholar 

  • Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515

    Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    CAS  PubMed  PubMed Central  Google Scholar 

  • FAO (2001) Global forest resources assessment 2000. Main report, FAO, Rome

  • FAO (2010) Global forest resources assessment 2010. Main report, FAO, Rome

  • Fischer MC, Rellstab C, Leuzinger M, Roumet M, Gugerli F, Shimizu KK et al. (2017) Estimating genomic diversity and population differentiation—an empirical comparison of microsatellite and SNP variation in Arabidopsis halleri. BMC Genomics 18:69

    PubMed  PubMed Central  Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2010) Introduction to conservation genetics, 2nd edn. Cambridge University Press, Cambridge

    Google Scholar 

  • Frankham R, Ballou JD, Ralls K, Eldridge M, Dudash MR, Fenster CB et al. (2017) Genetic management of fragmented animal and plant populations. Oxford University Press, Oxford, UK

  • Fraser DJ, Debes PV, Bernatchez L, Hutchings JA (2014) Population size, habitat fragmentation, and the nature of adaptive variation in a stream fish. Proc R Soc B 281:20140370

    PubMed  Google Scholar 

  • Galetti M, Guevara R, Neves CL, Rodarte RR, Bovendorp RS, Moreira M et al. (2015) Defaunation affects the populations and diets of rodents in Neotropical rainforests. Biol Conserv 190:2–7

    Google Scholar 

  • Galochet M, Morel V (2015) La biodiversité dans l’aménagement du territoire en Guyane française. VertigO – la revue électronique en sciences de l’environnement, Volume 15 Numéro 1. http://journals.openedition.org/vertigo/16069

  • Garnier S, Alibert P, Audiot P, Prieur B, Rasplus J-Y (2004) Isolation by distance and sharp discontinuities in gene frequencies: implications for the phylogeography of an alpine insect species, Carabus solieri. Mol Ecol 13:1883–1897

    CAS  PubMed  Google Scholar 

  • Garrick RC, Sunnucks P, Dyer RJ (2010) Nuclear gene phylogeography using PHASE: dealing with unresolved genotypes, lost alleles, and systematic bias in parameter estimation. BMC Evol Biol 10:118

    PubMed  PubMed Central  Google Scholar 

  • Gavan MK, Oliver MK, Douglas A, Piertney SB (2015) Gene dynamics of toll-like receptor 4 through a population bottleneck in an insular population of water voles (Arvicola amphibius). Conserv Genet 16:1181–1193

    CAS  Google Scholar 

  • Gonzalez-Quevedo C, Davies RG, Phillips KP, Spurgin LG, Richardson DS (2016) Landscape-scale variation in an anthropogenic factor shapes immune gene variation within a wild population. Mol Ecol 25:4234–4246

    CAS  PubMed  Google Scholar 

  • Gonzalez-Quevedo C, Spurgin LG, Illera JC, Richardson DS (2015) Drift, not selection, shapes toll-like receptor variation among oceanic island populations. Mol Ecol 24:5852–5863

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gottdenker NL, Streicker DG, Faust CL, Carroll CR (2014) Anthropogenic land use change and infectious diseases: a review of the evidence. EcoHealth 11:619–632

    PubMed  Google Scholar 

  • Grueber CE, Knafler GJ, King TM, Senior AM, Grosser S, Robertson B et al. (2015) Toll-like receptor diversity in 10 threatened bird species: relationship with microsatellite heterozygosity. Conserv Genet 16:595–611

    CAS  Google Scholar 

  • Grueber CE, Wallis GP, Jamieson IG (2013) Genetic drift outweighs natural selection at toll-like receptor (TLR) immunity loci in a re-introduced population of a threatened species. Mol Ecol 22:4470–4482

    CAS  PubMed  Google Scholar 

  • Grueber CE, Wallis GP, Jamieson IG (2014) Episodic positive selection in the evolution of avian toll-like receptor innate immunity genes. PLoS ONE 9:e89632

    PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guglielmone AA, Robbins RG, Apanaskevich DA, Petney TN, Estrada-Peña A, Horak IG (2014) The hard ticks of the world. Springer Netherlands, Dordrecht

    Google Scholar 

  • Haddad NM, Brudvig LA, Clobert J, Davies KF, Gonzalez A, Holt RD et al. (2015) Habitat fragmentation and its lasting impact on Earth’s ecosystems. Sci Adv 1:e1500052

    PubMed  PubMed Central  Google Scholar 

  • Hansen MC, Potapov PV, Moore R, Hancher M, Turubanova SA, Tyukavina A et al. (2013) High-resolution global maps of 21st-century forest cover change. Science 342:850–853

    CAS  PubMed  Google Scholar 

  • Harrisson KA, Pavlova A, Amos JN, Takeuchi N, Lill A, Radford JQ et al. (2013) Disrupted fine-scale population processes in fragmented landscapes despite large-scale genetic connectivity for a widespread and common cooperative breeder: the superb fairy-wren (Malurus cyaneus). J Anim Ecol 82:322–333

    PubMed  Google Scholar 

  • Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633–1638

    CAS  PubMed  Google Scholar 

  • Hillis DM, Moritz C, Mable BK (eds) (1996) Molecular systematics, 2nd ed. Sinauer Associates, Sunderland, Massachusetts

  • Holderegger R, Kamm U, Gugerli F (2006) Adaptive vs. neutral genetic diversity: implications for landscape genetics. Landsc Ecol 21:797–807

    Google Scholar 

  • Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332

    PubMed  PubMed Central  Google Scholar 

  • INSEE (2019) La population guyanaise à l’horizon 2050 : vers un doublement de la population? INSEE Antilles-Guyane, Pointe-à-pitre

  • Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL et al. (2008) Global trends in emerging infectious diseases. Nature 451:990–993

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jongejan F, Uilenberg G (2004) The global importance of ticks. Parasitology 129(Suppl):S3–S14

    PubMed  Google Scholar 

  • Kawai T, Akira S (2006) Innate immune recognition of viral infection. Nat Immunol 7:131–137

    CAS  PubMed  Google Scholar 

  • Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S et al. (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649

    PubMed  PubMed Central  Google Scholar 

  • Keesing F, Brunner J, Duerr S, Killilea M, LoGiudice K, Schmidt K et al. (2009) Hosts as ecological traps for the vector of Lyme disease. Proc R Soc B Biol Sci 276:3911–3919

    CAS  Google Scholar 

  • Keestra AM, de Zoete MR, Bouwman LI, Vaezirad MM, van Putten JPM (2013) Unique features of chicken toll-like receptors. Dev Comp Immunol 41:316–323

    CAS  PubMed  Google Scholar 

  • Keyghobadi N (2007) The genetic implications of habitat fragmentation for animals. Can J Zool 85:1049–1064

    Google Scholar 

  • Khimoun A, Arnoux E, Martel G, Pot A, Eraud C, Condé B et al. (2016b) Contrasted patterns of genetic differentiation across eight bird species in the Lesser Antilles. Genetica 144:125–138

    PubMed  Google Scholar 

  • Khimoun A, Eraud C, Ollivier A, Arnoux E, Rocheteau V, Bely M et al. (2016a) Habitat specialization predicts genetic response to fragmentation in tropical birds. Mol Ecol 25:3831–3844

    PubMed  Google Scholar 

  • Khimoun A, Ollivier A, Faivre B, Garnier S (2017) Level of genetic differentiation affects relative performances of expressed sequence tag and genomic SSRs. Mol Ecol Resour 17:893–903

    CAS  PubMed  Google Scholar 

  • Knafler GJ, Grueber CE, Sutton JT, Jamieson IG (2017) Differential patterns of diversity at microsatellite, MHC, and TLR loci in bottlenecked South Island saddleback populations. NZ J Ecol 41:98–106

    Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K, Battistuzzi FU (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lehmann T (1993) Ectoparasites: direct impact on host fitness. Parasitol Today 9:8–13

    CAS  PubMed  Google Scholar 

  • Lesica P, Allendorf FW (1995) When are peripheral populations valuable for conservation? Conserv Biol 9:753–760

    Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    CAS  PubMed  Google Scholar 

  • Lindenmayer DB, Fischer J (2013) Habitat fragmentation and landscape change: an ecological and conservation synthesis. Island Press, Washington, DC

  • Lindsay DL, Barr KR, Lance RF, Tweddale SA, Hayden TJ, Leberg PL (2008) Habitat fragmentation and genetic diversity of an endangered, migratory songbird, the golden-cheeked warbler (Dendroica chrysoparia). Mol Ecol 17:2122–2133

    PubMed  Google Scholar 

  • Losos JB, Ricklefs RE (2009) The theory of island biogeography revisited. Princeton University Press, Princeton

  • Marantz CA, Aleixo A, Bevier LR, Patten MA, Christie DA (2019) wedge-billed woodcreeper (Glyphorynchus spirurus). In: Handbook of the birds of the world alive. Lynx Edicions, Barcelona

  • McKay JK, Latta RG (2002) Adaptive population divergence: markers, QTL and traits. Trends Ecol Evolution 17:285–291

    Google Scholar 

  • Milá B, Bardeleben C (2005) Isolation of polymorphic tetranucleotide microsatellite markers for the wedge-billed woodcreeper Glyphorynchus spirurus. Mol Ecol Notes 5:844–845

    Google Scholar 

  • Minias P, Pikus E, Whittingham LA, Dunn PO (2018) A global analysis of selection at the avian MHC. Evolution 72:1278–1293

    PubMed  Google Scholar 

  • Murrell B, Moola S, Mabona A, Weighill T, Sheward D, Pond K et al. (2013) FUBAR: a fast, unconstrained bayesian approximation for inferring selection. Mol Biol Evol 30:1196–1205

    CAS  PubMed  PubMed Central  Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, O’hara RB, Simpson GL et al. (2019) Vegan: community ecology package, vol 2. R package version, p 5–6

  • Oliveira CJF, Carvalho WA, Garcia GR, Gutierrez FRS, de Miranda Santos IKF, Silva JS et al. (2010) Tick saliva induces regulatory dendritic cells: MAP-kinases and toll-like receptor-2 expression as potential targets. Vet Parasitol 167:288–297

    CAS  PubMed  Google Scholar 

  • ONF (2017) Occupation du sol 2015 sur la bande littorale de Guyane et son evolution entre 2005 et 2015. Direction Régionale ONF Guyane, Cayenne

  • Ostfeld RS, Keesing F, Eviner VT (2010) Infectious disease ecology: effects of ecosystems on disease and of disease on ecosystems. Princeton University Press, Princeton

  • Palumbi SR (2001) Humans as the world’s greatest evolutionary force. Science 293:1786–1790

    CAS  PubMed  Google Scholar 

  • Parham P (2003) Innate immunity: the unsung heroes. Nature 423:20

  • Patz JA, Graczyk TK, Geller N, Vittor AY (2000) Effects of environmental change on emerging parasitic diseases. Int J Parasitol 30:1395–1405

    CAS  PubMed  Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pearson SK, Bull CM, Gardner MG (2018) Selection outweighs drift at a fine scale: lack of MHC differentiation within a family living lizard across geographically close but disconnected rocky outcrops. Mol Ecol 27:2204–2214

    PubMed  Google Scholar 

  • Pond SLK, Frost SDW (2005) Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21:2531–2533

    CAS  PubMed  Google Scholar 

  • Porlier M, Garant D, Perret P, Charmantier A (2012) Habitat-linked population genetic differentiation in the blue tit Cyanistes caeruleus. J Hered 103:781–791

    PubMed  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 

  • Quéméré E, Hessenauer P, Galan M, Fernandez M, Merlet J, Chaval Y et al. (2018) Fluctuating pathogen-mediated selection favours the maintenance of innate immune gene polymorphism in a widespread wild ungulate. bioRxiv: https://doi.org/10.1101/458216

  • R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, R Core Team, Vienna

  • Radwan J, Kuduk K, Levy E, LeBas N, Babik W (2014) Parasite load and MHC diversity in undisturbed and agriculturally modified habitats of the ornate dragon lizard. Mol Ecol 23:5966–5978

    CAS  PubMed  Google Scholar 

  • Richardson JL, Urban MC, Bolnick DI, Skelly DK (2014) Microgeographic adaptation and the spatial scale of evolution. Trends Ecol Evol 29:165–176

    PubMed  Google Scholar 

  • Rivera-Ortíz FA, Aguilar R, Arizmendi MDC, Quesada M, Oyama K (2015) Habitat fragmentation and genetic variability of tetrapod populations: fragmentation and genetic variability. Anim Conserv 18:249–258

    Google Scholar 

  • Rousset F (2008) genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–106

    PubMed  Google Scholar 

  • Sagonas K, Runemark A, Antoniou A, Lymberakis P, Pafilis P, Valakos ED et al. (2019) Selection, drift, and introgression shape MHC polymorphism in lizards. Heredity 122:468–484

    CAS  PubMed  Google Scholar 

  • Sano E, Carlson S, Wegley L, Rohwer F (2004) Movement of viruses between biomes. Appl Environ Microbiol 70:5842–5846

    CAS  PubMed  PubMed Central  Google Scholar 

  • Santonastaso T, Lighten J, van Oosterhout C, Jones KL, Foufopoulos J, Anthony NM (2017) The effects of historical fragmentation on major histocompatibility complex class II β and microsatellite variation in the Aegean island reptile, Podarcis erhardii. Ecol Evol 7:4568–4581

    PubMed  PubMed Central  Google Scholar 

  • Schleicher A, Biedermann R, Kleyer M (2011) Dispersal traits determine plant response to habitat connectivity in an urban landscape. Landsc Ecol 26:529–540

    Google Scholar 

  • Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18:233–234

    CAS  PubMed  Google Scholar 

  • Seutin G, White BN, Boag PT (1991) Preservation of avian blood and tissue samples for DNA analyses. Can J Zool 69:82–90

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Spielman D, Brook BW, Frankham R (2004) Most species are not driven to extinction before genetic factors impact them. PNAS 101:15261–15264

    CAS  PubMed  Google Scholar 

  • Spurgin LG, Richardson DS (2010) How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proc R Soc B Biol Sci 277:979–988

    CAS  Google Scholar 

  • Stephens M, Donnelly P (2003) A comparison of bayesian methods for haplotype reconstruction from population genotype data. Am J Hum Genet 73:1162–1169

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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? Ecol Evol 2:341–353

    PubMed  PubMed Central  Google Scholar 

  • Sunnucks P (2011) Towards modelling persistence of woodland birds: the role of genetics. Emu 111:19–39

    Google Scholar 

  • Szpiech ZA, Jakobsson M, Rosenberg NA (2008) ADZE: a rarefaction approach for counting alleles private to combinations of populations. Bioinformatics 24:2498–2504

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tschirren B (2015) Borrelia burgdorferi sensu lato infection pressure shapes innate immune gene evolution in natural rodent populations across Europe. Biol Lett 11:20150263

    PubMed  PubMed Central  Google Scholar 

  • Väli U, Einarsson A, Waits L, Ellegren H (2008) To what extent do microsatellite markers reflect genome-wide genetic diversity in natural populations? Mol Ecol 17:3808–3817

    PubMed  Google Scholar 

  • Van Etten J (2017) R package gdistance: distances and routes on geographical grids. J Stat Softw 76:1–21

    Google Scholar 

  • Van Houtan KS, Pimm SL, Halley JM, Bierregaard RO, Lovejoy TE (2007) Dispersal of Amazonian birds in continuous and fragmented forest. Ecol Lett 10:219–229

    PubMed  Google Scholar 

  • Vilas A, Pérez-Figueroa A, Quesada H, Caballero A (2015) Allelic diversity for neutral markers retains a higher adaptive potential for quantitative traits than expected heterozygosity. Mol Ecol 24:4419–4432

    PubMed  Google Scholar 

  • Vinkler M, Albrecht T (2009) The question waiting to be asked: innate immunity receptors in the perspective of zoological research. Folia Zool 58:15

    Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    CAS  PubMed  Google Scholar 

  • Wlasiuk G, Nachman MW (2010) Adaptation and constraint at toll-like receptors in primates. Mol Biol Evol 27:2172–2186

    CAS  PubMed  PubMed Central  Google Scholar 

  • Woltmann S, Kreiser BR, Sherry TW (2012) Fine-scale genetic population structure of an understory rainforest bird in Costa Rica. Conserv Genet 13:925–935

    Google Scholar 

  • Yilmaz A, Shen S, Adelson DL, Xavier S, Zhu JJ (2005) Identification and sequence analysis of chicken toll-like receptors. Immunogenetics 56:743–753

    CAS  PubMed  Google Scholar 

  • Young HS, McCauley DJ, Dirzo R, Goheen JR, Agwanda B, Brook C et al. (2015) Context-dependent effects of large-wildlife declines on small-mammal communities in central Kenya. Ecol Appl 25:348–360

    PubMed  Google Scholar 


  • Source: Ecology - nature.com

    Effectiveness of protected areas in conserving tropical forest birds

    Did our early ancestors boil their food in hot springs?