Patagonian glacial effects on the endemic Green-backed Firecrown, Sephanoides sephaniodes (Aves: Trochilidae): evidence from species distribution models and molecular data

Abstract

Climate changes during the late Pleistocene influenced the demography and distribution of species in Patagonia. During the last glacial maximum (LGM), ice sheets covered a great extent of the temperate rainforest in the western Patagonian Andes. The persistence of forest species in refugia during the LGM has been debated for many vertebrates, but rarely for birds. The Green-backed Firecrown (Sephanoides sephaniodes) is an important avian pollinator distributed from the south of the Atacama Desert (28°S) to Tierra del Fuego (54°S) in South America. We evaluated the species’ evolutionary history, combining molecular data and models for past and current species distribution. Our results show two distinct haplogroups: the genetically diverse North–South clade (NS) restricted to the Mediterranean and coastal temperate regions that exhibits a signature of population expansion after LGM, and the Austral-East clade (AE) confined to the temperate intermountain range, eastern temperate, and sub-Antarctic regions, with lower genetic diversity and evidence of a more recent population expansion. This AE clade and the past distribution models support the species survival in valleys and lowlands south of the ice sheets limit during LGM until the present. A secondary contact zone was observed with haplotypes from the AE clade distributed in low frequency along with the northern areas. Our results support the paleorefugia hypothesis during the LGM with postglacial secondary contact.

Zusammenfassung

Auswirkungen der Eiszeit Patagoniens auf den endemischen Chilekolibri, Sephanoides sephaniodes (Aves: Trochilidae): Hinweise aus Artverbreitungsmodellen und molekularen Daten

Der Klimawandel während des späten Pleistozäns beeinflusste die Demographie und Verbreitung von Arten in Patagonien. Während des Letzteiszeitlichen Maximums (engl. last glacial maximum; LGM) bedeckten Eisschichten einen Großteil des gemäßigten Regenwaldes in den westlichen patagonischen Anden. Die Beharrlichkeit der Waldarten in Rückzugsgebieten während des LGMs wurde für viele Vertebraten-Arten diskutiert, jedoch selten für Vogelarten. Der Chilekolibri (Sephanoides sephaniodes) ist ein wichtiger Blütenbestäuber, der südlich der Atacamawüste (28°S) bis zum Feuerland (54°S) in Südamerika vorkommt. Wir untersuchten die Evolutionsgeschichte der Art, indem wir molekulare Daten und Modelle für die vergangene und derzeitige Artenverbreitung kombinierten. Unsere Ergebnisse zeigen zwei unterscheidbare Haplogruppen: die genetisch unterschiedliche Nord-Süd-Klade (NS), die auf mediterrane Regionen und gemäßigte Küstenregionen beschränkt ist und ein Zeichen einer Populationsverbreitung nach dem LGM zeigt, und die Süd-Ost-Klade (engl. Austral-East clade; AE), die sich auf die gemäßigte Intermountain Region sowie die östlichen gemäßigten und subantarktischen Regionen erstreckt, mit geringerer genetischer Vielfalt und mit Hinweise auf eine jüngere Populationsverbreitung. Diese AE-Klade und das Model für die vergangene Artenverbreitung belegen das Überleben der Arten in Tälern und Tiefebenen südlich der Grenze des Eisschildes während des LGMs bis zur Gegenwart. Eine sekundäre Kontaktzone wurde bei Haplogruppen der AE-Klade in dünn besiedelten nördlichen Regionen beobachtet. Unsere Ergebnisse unterstützen die Refugial-Hypothese während des LGMs mit postglazialen Sekundärkontakten.

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References

  1. Aizen MA, Vázquez DP, Smith-Ramírez C (2002) Historia natural y conservación de los mutualismos planta-animal del bosque templado de Sudamérica austral. Revista Chilena de História Natural 75:79–97

    Google Scholar 

  2. Aljanabi SM, Martinez I (1997) Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Res. 25:4692–4693

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    CAS  PubMed  Google Scholar 

  4. Benjamini Y, Krieger A, Yekutieli D (2006) Adaptive linear step-up procedures that control the false discovery rate. Biometrika 93:491–507

    Google Scholar 

  5. Brown JL, Bennett JR, French CM (2017) SDMtoolbox 2.0: the next generation Python-based GIS toolkit for landscape genetic, biogeographic and species distribution model analyses. Peer J 5:e4095. https://doi.org/10.7717/peerj.4095

    Article  PubMed  Google Scholar 

  6. Burridge CP, Craw D, Fletcher D, Waters JM (2008) Geological dates and molecular rates: fish DNA sheds light on time dependency. Mol Biol Evol 25:624–633

    CAS  PubMed  Google Scholar 

  7. Calderón L, Quintana F, Cabanne GS, Lougheed SC, Tubaro PL (2014) Phylogeography and genetic structure of two Patagonian shag species (Aves: Phalacrocoracidae). Mol Phylogenet Evol 72:42–53

    PubMed  Google Scholar 

  8. Campagna L, St Clair JH, Lougheed SC, Woods RW, Imberti S, Tubaro PL (2012) Divergence between passerine populations from the Malvinas—Falkland Islands and continental counterparts: a comparative phylogeographic study. Biol J Lin Soc 106:865–879

    Google Scholar 

  9. Cañón C, D’Elía G, Pardiñas UFJ, Lessa EP (2010) Phylogeography of Loxodontomys micropus with comments on the alpha taxonomy of Loxodontomys (Cricetidae: Sigmodontinae). J Mammal 91:1449–1458

    Google Scholar 

  10. Colwell RK (1989) Hummingbirds of the Juan Fernández Islands, natural history, evolution and population status. Ibis 131:548–566

    Google Scholar 

  11. Corander J. Lu C, Marttinen P, Sirén J & Tang J (2006). BAPS: Bayesian Analysis of Population Structure.

  12. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214

    PubMed  PubMed Central  Google Scholar 

  13. ESRI (2019) ArcGis Desktop, version 10.8. Environmental Systems Research Institute, Redlands, CA

  14. Excoffier L, Lischer HEL (2010) Arlequin suite version 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resources 10:564–567

    Google Scholar 

  15. Fraga M, Ruffini E, Grigera D (1997) Interacciones entre el picaflor rubí Sephanoides sephaniodes y plantas del bosque subantártico en el parque nacional Nahuel Huapi, Argentina. Hornero 14:224–234

    Google Scholar 

  16. Frugone MJ, Lowther A, Noll D, Ramos B, Pistorius P, Dantas GPM, Dantas MV, Petry F, Bonadonna A, Steinfurth A, Polanowski AR, Rey NA, Lois K, Pütz P, Trathan B, Wienecke EP, Vianna JA (2018) Contrasting phylogeographic pattern among Eudyptes penguins around the Southern Ocean. Sci Rep 8(1):17481

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Fuentes-Hurtado M, Marín JC, González-Acuña D, Verdugo C, Vidal F, Vianna JA (2011) Molecular divergence between insular and continental Pudu deer (Pudu puda) populations in the Chilean Patagonia. Stud Neotropical Fauna Environ 46:23–33

    Google Scholar 

  19. 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 

  20. González-Acuña D, Ardiles K, Welkner T, Cicchino A (2009) New data on the distribution of passeriform birds in the north of Chile. Boletín Chileno de Ornitol 15:23–28

    Google Scholar 

  21. González-Acuña D, Silva C, Soto M, Mironov S, Moreno L, González-Gómez PL, Badrul H, Kinsella M (2011) Parasites of the Green-backed Firecrown (Sephanoides sephaniodes) in Chile. Revista Mexicana de Biodiversidad 82(4):1333–1336

    Google Scholar 

  22. González-Acuña D, Mercado A, Valdes M, Rojas F, Najle M, Gallegos P, Doussang D, Cifuentes K, Martín N, Barrientos C (2019) Historial de las aves atendidas dutante los últimos 16 años en el centro de rehabilitación de fauna silvestre de la Universidad de Concepción, sur de Chile. Revista Chilena de Ornitol 25(2):62–77

    Google Scholar 

  23. González-Gómez PL, Estades CF (2009) Is natural selection promoting sexual dimorphism in the Green-backed Firecrown Hummingbird (Sephanoides sephaniodes)? J Ornithol 150:351–356

    Google Scholar 

  24. González-Gómez PL, Vásquez RA (2006) A field study of spatial memory in Green-backed Firecrown hummingbirds (Sephanoides sephaniodes). Ethology 112:790–795

    Google Scholar 

  25. González J, Wink M (2010) Genetic differentiation of the Thorn-tailed Rayadito Aphrastura spinicauda (Furnariidae: Passeriformes) revealed by ISSR profiles suggests multiple palaeorefugia and high recurrent gene flow. Ibis 152:761–774

    Google Scholar 

  26. Gutiérrez-Tapia P, Palma RE (2016) Integrating phylogeography and species distribution models: cryptic distributional responses to past climate change in an endemic rodent from the central Chile hotspot. Divers Distrib 22:638–650

    PubMed  PubMed Central  Google Scholar 

  27. Grigera D, Trejo A (2009) Aves continentales de las provincias del Neuquén, Río Negro y Chubut. Distribución y estado de conservación. Secretaría de Investigación del Centro Regional Universitario Bariloche. Universidad Nacional del Comahue

  28. Groot JJ, Groot CR (1966) Polen spectra from deep-sea sediments as indicators of climatic changes in Southern South America. Mar Geol 4:467–524

    Google Scholar 

  29. Guillot G, Santos F, Estoup A (2008) Analyzing georeferenced population genetics data with Geneland: a new algorithm to deal with null alleles and a friendly graphical user interface. Bioinformatics 24:1406–1407

    CAS  PubMed  Google Scholar 

  30. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    PubMed  Google Scholar 

  31. Hahn IJ, Vergara PM, Römer U (2011) Habitat selection and population trends in terrestrial bird species of Robinson Crusoe Island: habitat generalists versus forest specialists. Biodivers Conserv 20(12):2797

    Google Scholar 

  32. Heusser CJ (1983) Quaternary pollen record from laguna de Tagua Tagua, Chile. Science 219:1429–1432

    CAS  PubMed  Google Scholar 

  33. Heusser CJ, Heusser LE, Lowell TV (1999) Paleoecology of the southern Chilean lake district isla grande de Chiloe during middle-late Llanquihue glaciation and deglaciation. Geogr Ann 81:231–284

    Google Scholar 

  34. Hewitt GM (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913

    CAS  PubMed  Google Scholar 

  35. Hewitt GM (2004) Genetic consequences of climatic oscillations in the Quaternary. Philosophical Trans R Soc B Biol Sci 359:183–195

    CAS  Google Scholar 

  36. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978

    Google Scholar 

  37. Hulton N, Purves R, Mcculloch R, Sugden D, Bentley M (2002) The last glacial maximum and deglaciation in southern South America. Quatern Sci Rev 21:233–241

    Google Scholar 

  38. Jaramillo A, Burke P, Beadle D (2003) Aves de Chile. Christopher Helm, London

    Google Scholar 

  39. Lessa EP, D’Elia G, Pardinas UF (2010) Genetic footprints of late Quaternary climate change in the diversity of Patagonian-Fueguian rodents. Mol Ecol 19:3031–3037

    PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  41. López A, Bonasora MG (2017) Phylogeography, genetic diversity and population structure in a Patagonian endemic plant. AoB PLANTS 9:plx017

  42. Lougheed SC, Freeland JR, Handford P, Boag PT (2000) A molecular phylogeny of warbling-finches (Poospiza): paraphyly in a Neotropical emberizid genus. Mol Phylogenet Evol 17:367–378

    CAS  PubMed  Google Scholar 

  43. Lu GQ, Bernatchez L (1999) A study of fluctuating asymmetry in hybrids of dwarf and normal lakes whitefish ecotypes (Coregonus clupeaformis) from different glacial races. Heredity 83:742–747

    PubMed  Google Scholar 

  44. Luebert F, Weigend M (2014) Phylogenetic insights into Andean plant diversification. Front Ecol Evol 2:1–17

    Google Scholar 

  45. Luebert F, Pliscoff P (2017) Sinopsis bioclimática y vegetacional de Chile: Segunda Edición. Editorial Universitaria, Santiago

    Google Scholar 

  46. Marín JC, Varas V, Vila AR, López R, Orozco-Terwengel P, Corti P (2013) Refugia in Patagonian fjords and the eastern Andes during the last glacial maximum revealed by huemul (Hippocamelus bisulcus) phylogeographical patterns and genetic diversity. J Biogeogr 40:2285–2298

    Google Scholar 

  47. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Can Res 27:209–220

    CAS  Google Scholar 

  48. Martínez D, González G (2017) Las aves de Chile: guía de campo y breve historia natural, ISBN: 9789568426026, 540 p.

  49. Mata J, Erize F, Rumboll M (2006) Aves de Sudamérica: Guía de campo Collins Primera edición. Letemendia, Buenos Aires

    Google Scholar 

  50. Maturana CS, Segovia NI, González-Wevar CA, Díaz A, Rosenfeld S, Poulin E, Jackson JA, Convey P (2020) Evidence of strong small-scale population structure in the Antarctic freshwater copepod Boeckella poppei in lakes on Signy Island. Limnology and Oceanography, South Orkney Islands. https://doi.org/10.1002/lno.11435

    Book  Google Scholar 

  51. McCulloch RD, Bentley MJ, Purves RS, Hulton NRJ, Sugden DE, Clapperton CM (2000) Climatic inferences from glacial and paleoecological evidence at the last glacial termination, southern South America. J Quat Sci 15:409–417

    Google Scholar 

  52. Mills LS (2007) Conservation of Wildlife Populations. Wiley-Blackwell, Malden

    Google Scholar 

  53. Napolitano C, Johnson WE, Sanderson J, O’Brien SJ, Hoelzel AR, Freer R, Dunstone N, Ritland K, Ritland CE, Poulin E (2014) Phylogeography and population history of Leopardus guigna, the smallest American felid. Conservation Genet 15:631–653

    Google Scholar 

  54. Narosky T, Izurieta D (2003) Guía para la identificación de las aves de Argentina y Uruguay. Asociación Ornitológica del Plata. 340pp

  55. Ney G, Frederick K, Schul J (2018) A post-pleistocene calibrated mutation rate from insect museum specimens. PLoS Curr 13:10

    Google Scholar 

  56. Nuñez JJ, Wood NK, Rabanal FE, Fontanella FM, Sites JW Jr (2011) Amphibian phylogeography in the Antipodes: Refugia and postglacial colonization explain mitochondrial haplotype distribution in the Patagonian frog Eupsophus calcaratus (Cycloramphidae). Mol Phylogenet Evol 58:343–352

    PubMed  Google Scholar 

  57. Phillips SJ (2009) A brief tutorial on maxent. network of conservation educators and practitioners, center for biodiversity and conservation, American Museum of Natural History. Lessons Conservation 3:108–135

    Google Scholar 

  58. Phillips SJ, Anderson RP, Dudík M, Schapire RE, Blair ME (2017) Opening the black box: an open-source release of Maxent. Ecography 40:887–893

    Google Scholar 

  59. Pliscoff P, Fuentes-Castillo T (2011) Representativeness of terrestrial ecosystems in Chile’s protected area system. Environ Conserv 38:303–311

    Google Scholar 

  60. Posada D (2008) JModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256

    CAS  PubMed  Google Scholar 

  61. Provan J, Bennett KD (2008) Phylogeographic insights into cryptic glacial refugia. Trends Ecol Evol 23:564–571

    PubMed  Google Scholar 

  62. Prychitko TM, Moore WS (1997) The utility of DNA sequences of an intron from the beta-fibrinogen gene in phylogenetic analysis of woodpeckers (Aves: Picidae). Mol Phylogenet Evol 8:193–204

    CAS  PubMed  Google Scholar 

  63. Rabassa J, Coronato A, Salemme M (2005) Chronology of the late cenozoic patagonian glaciations and their correlation with biostratigraphic units of the Pampean region (Argentina). J S Am Earth Sci 20:81–103

    Google Scholar 

  64. Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Systematic Biology syy032

  65. Remsen DR Jr, Good DA (1996) Misuse of data from mist-net captures to assess relative abundance in bird populations. Auk 113:381–398

    Google Scholar 

  66. Remsen JV, Bonan A (2019) Handbook of the Birds of the World Alive (eds. del Hoyo, J., Elliot, A., Sargatal, J., Christie, D. A., & de Juana, E.), https://www.hbw.com/node/56401, https://birdsoftheworld.org/bow/species/chutap1/cur/introduction, (Lynx Edicions).

  67. Rohling EJ, Foster GL, Grant KM, Marino G, Roberts AP, Tamisiea ME, Williams F (2014) Sea-level and deep-sea-temperature variability over the past 5.3 million years. Nature 508:477–485

    CAS  PubMed  Google Scholar 

  68. Roy MY, Torres-Mura JC, Hertel F (1998) Evolution and history of hummingbirds (Aves: Trochilidae) from the Juan Fernández Islands. Chile IBIS 140(2):265–273

    Google Scholar 

  69. Rozzi R, Martínez D, Willson MF, Sabag C (1995) Avifauna of South American temperate forests. In: Armesto JJ, Villagrán C, Arroyo MK (eds) Ecología de los bosques nativos de Chile. Editorial Universitaria, Santiago, pp 135–152

    Google Scholar 

  70. Ruzzante DE, Walde SJ, Gosse JC, Cussac VE, Habit E, Zemlak TS, Adams EDM (2008) Climate control on ancestral population dynamics: insight from Patagonian fish phylogeography. Mol Ecol 17:2234–2244

    CAS  PubMed  Google Scholar 

  71. Ruzzante DE, Simons AP, McCracken GR, Habit E, Walde SJ (2020) Multiple drainage reversal episodes and glacial refugia in a Patagonian fish revealed by sequenced microsatellites. Proc R Soc B 287:20200468

    CAS  PubMed  Google Scholar 

  72. Saint Laurent R, Legault M, Benatchez L (2003) Divergent selection maintains adaptive differentiation despite high gene flow between sympatric rainbow smelt ecotypes (Omerus mordax Mitchill). Mol Ecol 12:315–330

    CAS  PubMed  Google Scholar 

  73. Schönswetter P, Stehlik I, Holderegger R, Tribsch A (2005) Molecular evidence for glacial refugia of mountain plants in the European Alps. Mol Ecol 14:3547–3555

    Google Scholar 

  74. Sersic A, Cosacov A, Cocucci AA, Johnson LA, Pozner R, Avila LJ, Sites JW, Morando M (2011) Emerging phylogeographic patterns of plants and terrestrial vertebrates from Patagonia. Biol J Lin Soc 103:475–494

    Google Scholar 

  75. Smith-Ramírez C (2004) The Chilean coastal range: a vanishing center of biodiversity and endemism in South American temperate rainforests. Biodiversity Conservation 13:373–393

    Google Scholar 

  76. Soltis DE, Morris AB, McLachlan JS, Manos PS, Soltis PS (2006) Comparative phylogeography of unglaciated eastern North America. Mol Ecol 15:4261–4293

    PubMed  Google Scholar 

  77. Stuessy TF, Foland KA, Sutter JF, Sanders RW, Silva OM (1984) Botanical and geological significance of potassium-argon dates from the Juan Fernández Islands. Science 225:49–51

    CAS  PubMed  Google Scholar 

  78. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Tecklin DR, DellaSala DA, Luebert F, Pliscoff P (2011) Valdivian temperate rainforests of Chile and Argentina. In: DellaSala DA (ed) Temperate and boreal rainforests of the world: ecology and conservation. Island Press/Center for Resource Economics, Washington, pp 132–153

    Google Scholar 

  80. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin J, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882

    Google Scholar 

  81. Trujillo-Arias N, Dantas GPM, Arbeláez-Cortés E, Naokie K, Gómez MI, Santos FR, Miyaki CI, Aleixo A, Tubaro PL, Cabanne GS (2017) The niche and phylogeography of a passerine reveal the history of biological diversification between the Andean and the Atlantic forests. Mol Phylogenet Evol 112:107–121

    PubMed  Google Scholar 

  82. Turgeon J, Bernatchez L (2003) Reticulate evolution and phenotypic diversity in North American ciscoes, Coregonus ssp. (Teleostei: Salmonidae): implications for the conservation of an evolutionary legacy. Conserv Genet 4:67–81

    CAS  Google Scholar 

  83. Vianna JA, Noll D, Moreno L, Silva C, Muñoz-Leal S, Najle M, González-Acuña D (2017a) Record of an alleged extinct rodent: molecular analyses of the endemic Octodon pacificus from Chile. J Mammal 98(2):456–463

    Google Scholar 

  84. Vianna JA, Noll D, Dantas GPM, Petry MV, Barbosa A, González-Acuña D, Le Bohec C, Bonadonna F, Poulin E (2017b) Marked phylogeographic structure of Gentoo penguin reveals an ongoing diversification process along the Southern Ocean. Mol Phylogenet Evol 107:486–498

    PubMed  Google Scholar 

  85. Vianna JA, Medina-Vogel G, Chehébar C, Sielfeld W, Olavarría C, Faugeron S (2011) Phylogeography of the Patagonian otter Lontra provocax: adaptive divergence to marine habitat or signature of southern glacial refugia? BMC Evol Biol 11:53–65

    PubMed  PubMed Central  Google Scholar 

  86. Victoriano PF, Ortiz JC, Benavides E, Adams BJ, Sites JW (2008) Comparative phylogeography of codistributed species of Chilean Liolaemus (Squamata: Tropiduridae) from the central-southern Andean range. Mol Ecol 17:2397–2416

    CAS  PubMed  Google Scholar 

  87. Villagrán C (2001) Un modelo de la historia de la vegetación de la Cordillera de La Costa de Chile central-sur: la hipótesis glacial de Darwin. Revista Chilena de Historia Natural 74:793–803

    Google Scholar 

  88. Villagrán C, Moreno P, Villa R (1995) Ecología De Los Bosques Nativos De Chile, J. J. Armesto, C. Villagrán, M. K. Arroyo, Eds. (Editorial Universitaria, Universidad de Chile, Santiago, Chile, 1995), pp. 51–69

  89. Walsh JC, Venter O, Watson JE, Fuller RA, Blackburn TM, Possingham HP (2012) Exotic species richness and native species endemism increase the impact of exotic species on islands. Glob Ecol Biogeogr 21:841–850

    Google Scholar 

  90. Weir JT, Schluter D (2008) Calibrating the avian molecular clock. Mol Ecol 17:2321–2328

    CAS  PubMed  Google Scholar 

  91. Weider LJ, Hobæk A (2000) Facing North: investigating the northern dimension to biodiversity. Ann Zool Fenn 37:217–231

    Google Scholar 

  92. Xu JW, Pérez-Losada M, Jara CG, Crandall KA (2009) Pleistocene glaciation leaves deep signature on the freshwater crab Aegla alacalufi in Chilean Patagonia. Mol Ecol 18:904–918

    CAS  PubMed  Google Scholar 

  93. Yahnke CJ, Johnson WE, Geffen E, Smith D, Hertel F, Roy MS, Wayne RK (1996) Darwin’s fox: a distinct endangered species in a vanishing habitat. Conserv Biol 10:366–375

    Google Scholar 

  94. Zemlak TS, Walde SJ, Habit E, Ruzzante DE (2011) Climate-induced changes to the ancestral population size of two Patagonian galaxiids: the influence of glacial cycling. Mol Ecol 20:5280–5294

    PubMed  Google Scholar 

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Acknowledgements

Financial support for this study was provided by Fondecyt 1181677 and 1170972, Chile, and by CONICET, Argentina. This research has received funding from the European Union's H2020 research and innovation program under the Marie Sklodowska-Curie grant agreement No. 691149 (SuFoRun), MSCA-RISE-2015 (H2020 Marie Skłodowska-Curie Actions) . We thank Cynthia Wang-Claypool and Nicolas Segovia for the suggestions and the figure design. DNA sequences are available in GenBank (access number for Cytb MT640054-MT640101 and FIB7 MT636394-MT636457). Occurrence records table file and Maxent models in raster format have been deposited in the Zenodo online repository (https://doi.org/10.5281/zenodo.3893976).

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Acosta, I., Cabanne, G.S., Noll, D. et al. Patagonian glacial effects on the endemic Green-backed Firecrown, Sephanoides sephaniodes (Aves: Trochilidae): evidence from species distribution models and molecular data. J Ornithol 162, 289–301 (2021). https://doi.org/10.1007/s10336-020-01822-4

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Keywords

  • Patagonia
  • Glacial refugia
  • Valdivian temperate rainforest
  • Green-backed Firecrown