Historia biogeográfica del Gran Chaco: modelado de nicho y filogeografía de la Monterita Cabeza Negra (Microspingus melanoleucus) (Aves: Thraupidae)

Bárbara R. Delgado; Virginia Y. Mogni; Natalia Trujillo-Arias; Gustavo S. Cabanne

doi:10.56178/eh.v36i2.374

Articles Published 01 December 2021 https://doi.org/10.56178/eh.v36i2.374

Biogeography of the Gran Chaco: niche modeling and phylogeography of Microspingus melanoleucus (aves: Thraupidae)

Ecological Niche Modeling Gran Chaco Microspingus Phylogeography Pleistocene

Bárbara R. Delgado División de Ornitología, Museo Argentino de Ciencias Naturales “Bernardino Rivadavia” – CONICET. Av. Angel Gallardo 470, 1405 CABA, Argentina

Virginia Y. Mogni Cátedra de Botánica, Facultad de Ciencias Agrarias, Universidad Nacional de Rosario. Parque Villarino, CC Nº 14, 2125 Zavalla, Santa Fe, Argentina

Natalia Trujillo-Arias Grupo de Estudios en Biodiversidad, Universidad Industrial de Santander. Cl. 9 #Cra 27, Bucaramanga, Santander, Colombia

Gustavo S. Cabanne División de Ornitología, Museo Argentino de Ciencias Naturales “Bernardino Rivadavia” – CONICET. Av. Angel Gallardo 470, 1405 CABA, Argentina

Abstract

The Gran Chaco, which is part of the diagonal of Neotropical open formations, is a fundamental region to test hypotheses of past connections among the Atlantic Forest, the Amazon and the Yungas. The aim of this study was to evaluate whether the Gran Chaco was fragmented by expansions of wet forests during Pleistocene climatic oscillations, which could have connected the Atlantic Forest and the Yungas’s southern sector (Tucuman-Bolivian Forest). To test the hypothesis, we studied an endemic bird of the region, the Black-capped Warbling Finch (Microspingus melanoleucus). We conducted phylogeographic analyses employing DNA sequences of nuclear and mitochondrial markers, as well as ecological niche modeling (ENM) for the present and past periods (Last Interglacial, Last Glacial Maximum and Middle Holocene). The results indicated high gene flow among the studied populations, with no geographically restricted lineages. The niche models showed a relatively conserved distribution range across historic periods, although they suggested for the present, and particularly for the Mid Holocene, a lack of habitat suitability along a geographic diagonal from northeast to the southwest of the study region. These results supported temporal habitat stability in the Gran Chaco ecoregion, and did not support the hypothesis of expansions of wet-forests that could have fragmented the region and linked neighboring domains such as Andean and Atlantic forests.

PDF (Spanish)

References

AB'SABER AN (1977) Espaços ocupados pela expansão dos climas secos na América do Sul, por ocasião dos períodos glaciais quaternários. Paleoclimas 3:1-19.
ANDERSON D, ANDERSON DE, GOUDIE A y PARKER A (2013) Global environments through the quaternary: exploring environmental change. Oxford University Press, Oxford.
BANDELT HJ, FORSTER P y RÖHL A (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16:37-48.
BATALHA-FILHO H, CABANNE GS y MIYAKI CY (2012) Phylogeography of an Atlantic forest passerine reveals demographic stability through the last glacial maximum. Molecular Phylogenetics and Evolution 65:892-902.
BEHLING H y HOOGHIEMSTRA H (1998) Late Quaternary palaeoecology and palaeoclimatology from pollen records of the savannas of the Llanos Orientales in Colombia. Palaeogeography, Palaeoclimatology, Palaeoecology 139:251-267.
BILLERMAN SM, KEENEY BK, RODEWALD PG y SCHULENBERG TS (eds.) (2020) Birds of the World. Cornell Laboratory of Ornithology, Ithaca (URL: https://birdsoftheworld.org/bow/home).
BORGE T, WEBSTER MT, ANDERSSON G y SAETRE GP (2005) Contrasting patterns of polymorphism and divergence on the Z chromosome and autosomes in two Ficedula flycatcher species. Genetics 171:1861-1873.
BOUCKAERT R, VAUGHAN TG, BARIDO-SOTTANI J, DUCHÊNE S, FOURMENT M, GAVRYUSHKINA A, HELED J, JONES G, KÜHNERT D, DE MAIO N, MATSCHINER M, MENDES FK, MÜLLER NF, OGILVIE HA, DU PLESSIS L, POPINGA A, RAMBAUT A, RASMUSSEN D, SIVERONI I, SUCHARD MA, WU C, XIE D, ZHANG C, STADLER T y DRUMMOND AJ (2019) BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLoS Computational Biology 15:e1006650.
BROECKER WS y VAN DONK J (1970) Insolation changes, ice volumes, and the O18 record in deepsea cores. Reviews of Geophysics 8:169-198.
BRUNETTO E, FERRERO B y NORIEGA JI (2015) Late Pleistocene lithostratigraphy and sequences in the southwestern Mesopotamia (Argentina): evidences of the Last Interglacial Stage. Journal of South American Earth Sciences 58:111-128.
BRUSQUETTI F, NETTO F, BALDO D y HADDAD CF (2018) What happened in the South American Gran Chaco? Diversification of the endemic frog genus Lepidobatrachus Budgett, 1899 (Anura: Ceratophryidae). Molecular Phylogenetics and Evolution 123:123-136.
BRUSQUETTI F, NETTO F, BALDO D y HADDAD CF (2019) The influence of Pleistocene glaciations on Chacoan fauna: genetic structure and historical demography of an endemic frog of the South American Gran Chaco. Biological Journal of the Linnean Society 126:404-416.
BURNS KJ, SHULTZ AJ, TITLE PO, MASON NA, BARKER FK, KLICKA J, LANYON SM y LOVETTE IJ (2014) Phylogenetics and diversification of tanagers (Passeriformes: Thraupidae), the largest radiation of Neotropical songbirds. Molecular Phylogenetics and Evolution 75:41-77.
CABANNE GS, CAMPAGNA L, TRUJILLO-ARIAS N, NAOKI K, GOMEZ I, MIYAKI CY, SANTOS FR, DANTAS GPM, ALEIXO A, CLARAMUNT S, ROCHA A, CAPARROZ R, LOVETTE IJ y TUBARO PL (2019) Phylogeographic variation within the Buff-browed Foliage-gleaner (Aves: Furnariidae: Syndactyla rufosuperciliata) supports an Andean-Atlantic forests connection via the Cerrado. Molecular Phylogenetics and Evolution 133:198-213.
CAMPS GA, MARTÍNEZ-MEYER E, VERGA AR, SERSIC AN y COSACOV A (2018) Genetic and climatic approaches reveal effects of Pleistocene refugia and climatic stability in an old giant of the Neotropical Dry Forest. Biological Journal of the Linnean Society 125:401-420.
CARNAVAL AC y MORITZ C (2008) Historical climate modelling predicts patterns of current biodiversity in the Brazilian Atlantic forest. Journal of Biogeography 35:1187-1201.
CHAN LM, BROWN JL y YODER AD (2011) Integrating statistical genetic and geospatial methods brings new power to phylogeography. Molecular Phylogenetics and Evolution 59:523-537.
CLARK PU, ARCHER D, POLLARD D, BLUM JD, RIAL JA, BROVKIN V, MIX AC, PISIAS NG y ROY M (2006) The middle Pleistocene transition: characteristics, mechanisms, and implications for long-term changes in atmospheric pCO2. Quaternary Science Reviews 25:3150-3184.
CONTRERAS SA y ZUCOL AF (2019) Late Quaternary vegetation history based on phytolith records in the eastern Chaco (Argentina). Quaternary International 505:21-33.
DARRIBA D, TABOADA GL, DOALLO R y POSADA D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9:772.
DINERSTEIN E, OLSON D, JOSHI A, VYNNE, C, BURGESS ND, WIKRAMANAYAKE E, HAHN N, PALMINTERI S, HEDAO P, NOSS R, HANSEN M, LOCKE H, ELLIS EC, JONES B, BARBER CV, HAYES R, KORMOS C, MARTIN V, CRIST E, SECHREST W, PRICE L, BAILLIE JEM, WEEDEN D, SUCKLING K, DAVIS C, SIZER N, MOORE R, THAU D, BIRCH T, POTAPOV P, TURUBANOVA S, TYUKAVINA A, DE SOUZA N, PINTEA L, BRITO JC, LLEWELLYN OA, MILLER AG, PATZELT A, GHAZANFAR SA, TIMBERLAKE J, KLÖSER H, SHENNAN-FARPÓN Y, KINDT R, BARNEKOW LILLES JP, VAN BREUGEL P, GRAUDAL L, VOGE M, AL-SHAMMARI KF y SALEEM M (2017) An Ecoregion-Based Approach to Protecting Half the Terrestrial Realm. BioScience 1:1-12.
EBIRD (2021) eBird: An online database of bird distribution and abundance (web application). eBird, Cornell Lab of Ornithology, Ithaca (URL: http://www.ebird.org).
EXCOFFIER L y LISCHER H (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10:564-567.
FERRERO BS, NORIEGA JI, BRUNETTO E y OTAÑO NN (2017) Vertebrate continental assemblage from the last interglacial in southern South America (Entre Ríos, Argentina). Biostratigraphy and paleoenvironment. Palaeogeography, Palaeoclimatology, Palaeoecology 466:89-99.
FJELDSÅ J, ZUCCON D, IRESTEDT M, JOHANSSON US y ERICSON P (2003) Sapayoa aenigma: a New World representative of Old World suboscines. Proceeding of the Royal Society of London 270:S238-S241.
Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915-25.
GENT PR, DANABASOGLU G, DONNER LJ, HOLLAND MM, HUNKE EC, JAYNE SR, LAWRENCE DM, NEALE RB, RASCH PJ y VERTENSTEIN M (2011) The community climate system model version 4. Journal of climate 24:4973-4991.
GRAHAM CH, MORITZ C y WILLIAMS SE (2006) Habitat history improves prediction of biodiversity in rainforest fauna. Proceedings of the National Academy of Sciences 103:632-636.
GRAHAM CH, MORITZ C y WILLIAMS SE (2006) Habitat history improves prediction of biodiversity in rainforest fauna. Proceedings of the National Academy of Sciences 103:632-636.
GRIFFITHS R, DOUBLE M, ORR K y DAWSON R (1998) A DNA test to sex most birds. Molecular Ecology 7:1071-1075.
GUILLOT G, MORTIER F y ESTOUP A (2005) Geneland: A program for landscape genetics. Molecular Ecology Notes 5:712-715.
HAFFER J (1969) Speciation in Amazonian forest birds. Science 165:131-137.
HARRISON S y NOSS R (2017) Endemism hotspots are linked to stable climatic refugia. Annals of Botany 119:207-214.
HAYS JD, IMBRIE J y SHACKLETON NJ (1976) Variations in the Earth's orbit: pacemaker of the ice ages. Science 194:1121-1132.
HELED J y DRUMMOND AJ (2008) Bayesian inference of population size history from multiple loci. BMC Evolutionary Biology 8:289.
HIJMANS RJ, CAMERON SE, PARRA JL, JONES PG y JARVIS A (2005) Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology: A Journal of the Royal Meteorological Society 25:1965-1978.
HIJMANS R, GUARINO L, JARVIS A y O'BRIEN R (2007) DIVA-GIS v.7.5.0.0. (URL: http://www.diva-gis.org/).
IRIONDO M (1993) Geomorphology and late Quaternary of the Chaco (South America). Geomorphology 7:289-303.
IVANOVA NV, DEWAARD JR y HEBERT PDN (2006) An inexpensive, automation-friendly protocol for recovering high-quality DNA. Molecular Ecology Notes 6:998-1002.
KOPUCHIAN C, CAMPAGNA L, LIJTMAER DA, CABANNE GS, GARCÍA NC, LAVINIA PD, TUBARO PL, LOVETTE I y DI GIACOMO AS (2020) A test of the riverine barrier hypothesis in the largest subtropical river basin in the Neotropics. Molecular ecology 29:2137-2149.
KUMAR S, STECHER G, LI M, KNYAZ C y TAMURA K (2018) MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Molecular Biology and Evolution 35:1547-1549.
LEDRU MP (2002) Late Quaternary history and evolution of the Cerrados as revealed by palynological records. Pp. 33-50 en: OLIVEIRA PS y MARQUIS RJ (eds) The Cerrados of Brazil: Ecology and Natural History of a Neotropical Savanna. Columbia University Press, New York.
LOUGHEED S, FREELAND J, HANDFORD P y BOAG P (2000) A molecular phylogeny of Warbling-Finches (Poospiza): Paraphyly in a Neotropical emberizid genus. Molecular Phylogenetics and Evolution 17:367-378.
MAY JH, ARGOLLO J y VEIT H (2008) Holocene landscape evolution along the Andean piedmont, Bolivian Chaco. Palaeogeography, Palaeoclimatology, Palaeoecology 260:505-520.
MORENO ES, DE FREITAS LB, SPERANZA PR y SOLÍS NEFFA VG (2018) Impact of Pleistocene geoclimatic events on the genetic structure in mid-latitude South American plants: insights from the phylogeography of Turnera sidoides complex (Passifloraceae, Turneroideae). Botanical Journal of the Linnean Society 188:377-390.
MORITZ C, PATTON JL, SCHNEIDER CJ y SMITH TB (2000) Diversification of Rainforest Faunas: An Integrated Molecular Approach. Annual Review of Ecology and Systematics 31:533-563.
NAROSKY T y YZURIETA D (2010) Aves de Argentina y Uruguay. Vazquez Mazzini Editores, Buenos Aires.
NORES M (1992) Bird speciation in subtropical South America in relation to forest expansion and retraction. Auk 109:346-357.
OTTO-BLIESNER BL, MARSHALL SJ, OVERPECK JT, MILLER GH y Hu A (2006) Simulating Arctic climate warmth and icefield retreat in the last interglaciation. Science 311:1751-1753.
PAILLARD D (1998) The timing of Pleistocene glaciations from a simple multiple-state climate model. Nature 391:378-381.
PHILLIPS SJ, ANDERSON RP y SCHAPIRE RE (2006) Maximum entropy modeling of species geographic distributions. Ecological modelling 190:231-259.
PIOVANO EL, ARIZTEGUI D, CÓRDOBA F, CIOCCALE M y SYLVESTRE F (2009) Hydrological Variability in South America Below the Tropic of Capricorn (Pampas and Patagonia, Argentina) During the Last 13.0 Ka. Pp. 323-351 en: VIMEUX F, KHODRI M y SYLVESTRE F (eds.) Past Climate Variability in South America and Surrounding Regions: from the Last Glacial Maximum to the Holocene. Springer Science and Business Media, Berlin/Heidelberg.
PISIAS NG y MOORE TC (1981) The evolution of Pleistocene climate: A time series approach. Earth and Planetary Science Letters 52:450-458.
PRADO DE (1993) What is the Gran Chaco vegetation in South America? I. A review. Contribution to the study of flora and vegetation of the Chaco. V. Candollea 48:145-172.
PRADO LF, WAINER I, CHIESSI CM, LEDRU MP y TURCQ B (2013) A mid-Holocene climate reconstruction for eastern South America. Climate of the Past 9:2117-2133.
RAMBAUT A, DRUMMOND AJ, XIE D, BAELE G y SUCHARD MA (2018) Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67:901.
ROBBIATI FO, NORES MJ, ANTON AM y FORTUNATO RH (2021) Stability and fragmentation versus demographic expansion: different phylogeographic patterns in closely related sympatric legumes (Senna) from arid and semi-arid zones of mid-latitude South America. Botanical Journal of the Linnean Society 196:364-383.
ROCHA AV, CABANNE GS, ALEIXO A, SILVEIRA LF, TUBARO P y CAPARROZ R (2020) Pleistocene climatic oscillations associated with landscape heterogeneity of the South American dry diagonal explains the phylogeographic structure of the narrow-billed woodcreeper (Lepidocolaptes angustirostris, Dendrocolaptidae). Journal of Avian Biology 51(09):e02537.
ROZAS J, FERRER-MATA A, SÁNCHEZ-DELBARRIO JC, GUIRAO-RICO S, LIBRADO P, RAMOS-ONSINS SE y SÁNCHEZ-GRACIA A (2017) DnaSP v6: DNA Sequence Polymorphism Analysis of Large Datasets. Molecular Biology and Evolution 34:3299-3302.
R DEVELOPMENT CORE TEAM (2019) R: a language and environment for statistical computing (URL: http://www.R-project.org/).
SILVA JMC (1994) Can avian distribution patterns in Northern Argentina be related to retraction caused by Quaternary climatic changes? Auk 111:495-499.
SILVA JMC (1996) Distribution of Amazonian and Atlantic birds in gallery forests of the Cerrado region, South America. Ornitologia Neotropical 7:1-18.
SOBRAL-SOUZA T, LIMA-RIBEIRO MS y SOLFERINI VN (2015) Biogeography of Neotropical Rainforests: past connections between Amazon and Atlantic Forest detected by ecological niche modeling. Evolutionary Ecology 29:643-655.
STEPHENS M y DONNELLY P (2003) A comparison of bayesian methods for haplotype reconstruction. The American Journal of Human Genetics 73:1162-1169.
SYLVESTRE F (2009) Moisture Pattern During the Last Glacial Maximum in South America. Pp. 3-27 en: VIMEUX F, KHODRI M y SYLVESTRE F (eds.) Past Climate Variability in South America and Surrounding Regions: from the Last Glacial Maximum to the Holocene. Springer Science and Business Media, Berlin/Heidelberg.
TAJIMA F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585-595.
TRUJILLO-ARIAS N, DANTAS G, ARBELAEZ-CORTÉS E, NAOKI K, GÓMEZ MI, SANTOS FR, MIYAKI CY, ALEIXO A, TUBARO PL y CABANNE GS (2017) The niche and phylogeography of a passerine reveal the history of biological diversification between the Andean and the Atlantic forests. Molecular Phylogenetics and Evolution 112:107-121.
TRUJILLO-ARIAS N, CALDERÓN L, SANTOS FR, MIYAKI CY, ALEIXO A, WITT CC, TUBARO PL y CABANNE GS (2018) Forest corridors between the central Andes and the southern Atlantic Forest enabled dispersal and peripatric diversification without niche divergence in a passerine. Molecular Phylogenetics and Evolution 128:221-232.
TRUJILLO-ARIAS N, RODRÍGUEZ-CAJARVILLE MJ, SARI E, MIYAKI CY, SANTOS FR, WITT CC, BARREIRA AS, GOMEZ MI, NAOKI K, TUBARO PL y CABANNE GS (2020) Evolution between forest macrorefugia is linked to discordance between genetic and morphological variation in Neotropical passerines. Molecular Phylogenetics and Evolution 149:106849.
TURCHETTO-ZOLET AC, SALGUEIRO F, TURCHETTO C, CRUZ F, VETO NM, BARROS MJF, SEGATTO ALA, FREITAS LB y MARGIS R (2016) Phylogeography and ecological niche modelling in Eugenia uniflora (Myrtaceae) suggest distinct vegetational responses to climate change between the southern and the northern Atlantic Forest. Botanical Journal of the Linnean Society 182:670-688.
VUILLEUMIER BS (1971) Pleistocene Changes in the Fauna and Flora of South America. Science 173:771-780.
WATANABE S, HAJIMA T, SUDO K, NAGASHIMA T, TAKEMURA T, OKAJIMA H, NOZAWA T, KAWASE H, ABE M, YOKOHATA T, ISEL T, SATO H, KATO E, TAKATA K, EMORI S y KAWAMIYA M (2011) MIROC-ESM 2010: Model description and basic results of CMIP5-20c3m experiments. Geoscientific Model Development 4:845-872.
WEIR JT y SCHLUTER D (2008) Calibrating the avian molecular clock. Molecular ecology 17:2321-2328.
WERNECK FP (2011) The diversification of eastern South American open vegetation biomes: Historical biogeography and perspectives. Quaternary Science Reviews 30:1630-1648.
WORLDCLIM (2021) Climate Data for Modeling and GIS. URL: https://www.worldclim.org/data/index.html
XIE W, LEIGH JW, YANG Q, WANG B y RAO H (2011) Bayesian inference of species divergence times using correlated quantitative characters. Evolution 65:1081-1095.
YANG Z (2015) The BPP program for species tree estimation and species delimitation. Current Zoology 61:854-865.
ZUCKERKANDL E y PAULING L (1965) Evolutionary divergence and convergence in proteins. Pp. 97-166 en: BRYSON V y VOGEL HJ (eds.) Evolving Genes and Proteins. Academic Press, New York.
ZUCULET EA, ILSENHOUT AM y SCALABRINI A (2018) Modelos de distribución potencial para evaluar el efecto de cambios climáticos en la distribución de especies arbóreas del Bosque Atlántico. Ecología Austral 28:237-253.
ZUUR AF, IENO EN, WALKER NJ, SAVELIEV AA y SMITH GM (2009) Mixed Effects Models and Extensions in Ecology with R. Springer, New York.
ZUUR AF, LENO EN y ELPHICK CS (2010) A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution 1:3-14.

How to cite

Bárbara R. Delgado, Virginia Y. Mogni, Natalia Trujillo-Arias, Gustavo S. Cabanne (2021). Biogeography of the Gran Chaco: niche modeling and phylogeography of Microspingus melanoleucus (aves: Thraupidae). El Hornero, Vol. 36 No. 2 (2021), 107-120. https://doi.org/10.56178/eh.v36i2.374

Downloads

603Full-text views

1Formats

License: CC BY-NC 4.0

[1] AB'SABER AN (1977) Espaços ocupados pela expansão dos climas secos na América do Sul, por ocasião dos períodos glaciais quaternários. Paleoclimas 3:1-19.

[2] ANDERSON D, ANDERSON DE, GOUDIE A y PARKER A (2013) Global environments through the quaternary: exploring environmental change. Oxford University Press, Oxford.

[3] BANDELT HJ, FORSTER P y RÖHL A (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16:37-48.

[4] BATALHA-FILHO H, CABANNE GS y MIYAKI CY (2012) Phylogeography of an Atlantic forest passerine reveals demographic stability through the last glacial maximum. Molecular Phylogenetics and Evolution 65:892-902.

[5] BEHLING H y HOOGHIEMSTRA H (1998) Late Quaternary palaeoecology and palaeoclimatology from pollen records of the savannas of the Llanos Orientales in Colombia. Palaeogeography, Palaeoclimatology, Palaeoecology 139:251-267.

[6] BILLERMAN SM, KEENEY BK, RODEWALD PG y SCHULENBERG TS (eds.) (2020) Birds of the World. Cornell Laboratory of Ornithology, Ithaca (URL: https://birdsoftheworld.org/bow/home).

[7] BORGE T, WEBSTER MT, ANDERSSON G y SAETRE GP (2005) Contrasting patterns of polymorphism and divergence on the Z chromosome and autosomes in two Ficedula flycatcher species. Genetics 171:1861-1873.

[8] BOUCKAERT R, VAUGHAN TG, BARIDO-SOTTANI J, DUCHÊNE S, FOURMENT M, GAVRYUSHKINA A, HELED J, JONES G, KÜHNERT D, DE MAIO N, MATSCHINER M, MENDES FK, MÜLLER NF, OGILVIE HA, DU PLESSIS L, POPINGA A, RAMBAUT A, RASMUSSEN D, SIVERONI I, SUCHARD MA, WU C, XIE D, ZHANG C, STADLER T y DRUMMOND AJ (2019) BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLoS Computational Biology 15:e1006650.

[9] BROECKER WS y VAN DONK J (1970) Insolation changes, ice volumes, and the O18 record in deepsea cores. Reviews of Geophysics 8:169-198.

[10] BRUNETTO E, FERRERO B y NORIEGA JI (2015) Late Pleistocene lithostratigraphy and sequences in the southwestern Mesopotamia (Argentina): evidences of the Last Interglacial Stage. Journal of South American Earth Sciences 58:111-128.

[11] BRUSQUETTI F, NETTO F, BALDO D y HADDAD CF (2018) What happened in the South American Gran Chaco? Diversification of the endemic frog genus Lepidobatrachus Budgett, 1899 (Anura: Ceratophryidae). Molecular Phylogenetics and Evolution 123:123-136.

[12] BRUSQUETTI F, NETTO F, BALDO D y HADDAD CF (2019) The influence of Pleistocene glaciations on Chacoan fauna: genetic structure and historical demography of an endemic frog of the South American Gran Chaco. Biological Journal of the Linnean Society 126:404-416.

[13] BURNS KJ, SHULTZ AJ, TITLE PO, MASON NA, BARKER FK, KLICKA J, LANYON SM y LOVETTE IJ (2014) Phylogenetics and diversification of tanagers (Passeriformes: Thraupidae), the largest radiation of Neotropical songbirds. Molecular Phylogenetics and Evolution 75:41-77.

[14] CABANNE GS, CAMPAGNA L, TRUJILLO-ARIAS N, NAOKI K, GOMEZ I, MIYAKI CY, SANTOS FR, DANTAS GPM, ALEIXO A, CLARAMUNT S, ROCHA A, CAPARROZ R, LOVETTE IJ y TUBARO PL (2019) Phylogeographic variation within the Buff-browed Foliage-gleaner (Aves: Furnariidae: Syndactyla rufosuperciliata) supports an Andean-Atlantic forests connection via the Cerrado. Molecular Phylogenetics and Evolution 133:198-213.

[15] CAMPS GA, MARTÍNEZ-MEYER E, VERGA AR, SERSIC AN y COSACOV A (2018) Genetic and climatic approaches reveal effects of Pleistocene refugia and climatic stability in an old giant of the Neotropical Dry Forest. Biological Journal of the Linnean Society 125:401-420.

[16] CARNAVAL AC y MORITZ C (2008) Historical climate modelling predicts patterns of current biodiversity in the Brazilian Atlantic forest. Journal of Biogeography 35:1187-1201.

[17] CHAN LM, BROWN JL y YODER AD (2011) Integrating statistical genetic and geospatial methods brings new power to phylogeography. Molecular Phylogenetics and Evolution 59:523-537.

[18] CLARK PU, ARCHER D, POLLARD D, BLUM JD, RIAL JA, BROVKIN V, MIX AC, PISIAS NG y ROY M (2006) The middle Pleistocene transition: characteristics, mechanisms, and implications for long-term changes in atmospheric pCO2. Quaternary Science Reviews 25:3150-3184.

[19] CONTRERAS SA y ZUCOL AF (2019) Late Quaternary vegetation history based on phytolith records in the eastern Chaco (Argentina). Quaternary International 505:21-33.

[20] DARRIBA D, TABOADA GL, DOALLO R y POSADA D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9:772.

[21] DINERSTEIN E, OLSON D, JOSHI A, VYNNE, C, BURGESS ND, WIKRAMANAYAKE E, HAHN N, PALMINTERI S, HEDAO P, NOSS R, HANSEN M, LOCKE H, ELLIS EC, JONES B, BARBER CV, HAYES R, KORMOS C, MARTIN V, CRIST E, SECHREST W, PRICE L, BAILLIE JEM, WEEDEN D, SUCKLING K, DAVIS C, SIZER N, MOORE R, THAU D, BIRCH T, POTAPOV P, TURUBANOVA S, TYUKAVINA A, DE SOUZA N, PINTEA L, BRITO JC, LLEWELLYN OA, MILLER AG, PATZELT A, GHAZANFAR SA, TIMBERLAKE J, KLÖSER H, SHENNAN-FARPÓN Y, KINDT R, BARNEKOW LILLES JP, VAN BREUGEL P, GRAUDAL L, VOGE M, AL-SHAMMARI KF y SALEEM M (2017) An Ecoregion-Based Approach to Protecting Half the Terrestrial Realm. BioScience 1:1-12.

[22] EBIRD (2021) eBird: An online database of bird distribution and abundance (web application). eBird, Cornell Lab of Ornithology, Ithaca (URL: http://www.ebird.org).

[23] EXCOFFIER L y LISCHER H (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10:564-567.

[24] FERRERO BS, NORIEGA JI, BRUNETTO E y OTAÑO NN (2017) Vertebrate continental assemblage from the last interglacial in southern South America (Entre Ríos, Argentina). Biostratigraphy and paleoenvironment. Palaeogeography, Palaeoclimatology, Palaeoecology 466:89-99.

[25] FJELDSÅ J, ZUCCON D, IRESTEDT M, JOHANSSON US y ERICSON P (2003) Sapayoa aenigma: a New World representative of Old World suboscines. Proceeding of the Royal Society of London 270:S238-S241.

[26] Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915-25.

[27] GENT PR, DANABASOGLU G, DONNER LJ, HOLLAND MM, HUNKE EC, JAYNE SR, LAWRENCE DM, NEALE RB, RASCH PJ y VERTENSTEIN M (2011) The community climate system model version 4. Journal of climate 24:4973-4991.

[28] GRAHAM CH, MORITZ C y WILLIAMS SE (2006) Habitat history improves prediction of biodiversity in rainforest fauna. Proceedings of the National Academy of Sciences 103:632-636.

[29] GRAHAM CH, MORITZ C y WILLIAMS SE (2006) Habitat history improves prediction of biodiversity in rainforest fauna. Proceedings of the National Academy of Sciences 103:632-636.

[30] GRIFFITHS R, DOUBLE M, ORR K y DAWSON R (1998) A DNA test to sex most birds. Molecular Ecology 7:1071-1075.

[31] GUILLOT G, MORTIER F y ESTOUP A (2005) Geneland: A program for landscape genetics. Molecular Ecology Notes 5:712-715.

[32] HAFFER J (1969) Speciation in Amazonian forest birds. Science 165:131-137.

[33] HARRISON S y NOSS R (2017) Endemism hotspots are linked to stable climatic refugia. Annals of Botany 119:207-214.

[34] HAYS JD, IMBRIE J y SHACKLETON NJ (1976) Variations in the Earth's orbit: pacemaker of the ice ages. Science 194:1121-1132.

[35] HELED J y DRUMMOND AJ (2008) Bayesian inference of population size history from multiple loci. BMC Evolutionary Biology 8:289.

[36] HIJMANS RJ, CAMERON SE, PARRA JL, JONES PG y JARVIS A (2005) Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology: A Journal of the Royal Meteorological Society 25:1965-1978.

[37] HIJMANS R, GUARINO L, JARVIS A y O'BRIEN R (2007) DIVA-GIS v.7.5.0.0. (URL: http://www.diva-gis.org/).

[38] IRIONDO M (1993) Geomorphology and late Quaternary of the Chaco (South America). Geomorphology 7:289-303.

[39] IVANOVA NV, DEWAARD JR y HEBERT PDN (2006) An inexpensive, automation-friendly protocol for recovering high-quality DNA. Molecular Ecology Notes 6:998-1002.

[40] KOPUCHIAN C, CAMPAGNA L, LIJTMAER DA, CABANNE GS, GARCÍA NC, LAVINIA PD, TUBARO PL, LOVETTE I y DI GIACOMO AS (2020) A test of the riverine barrier hypothesis in the largest subtropical river basin in the Neotropics. Molecular ecology 29:2137-2149.

[41] KUMAR S, STECHER G, LI M, KNYAZ C y TAMURA K (2018) MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Molecular Biology and Evolution 35:1547-1549.

[42] LEDRU MP (2002) Late Quaternary history and evolution of the Cerrados as revealed by palynological records. Pp. 33-50 en: OLIVEIRA PS y MARQUIS RJ (eds) The Cerrados of Brazil: Ecology and Natural History of a Neotropical Savanna. Columbia University Press, New York.

[43] LOUGHEED S, FREELAND J, HANDFORD P y BOAG P (2000) A molecular phylogeny of Warbling-Finches (Poospiza): Paraphyly in a Neotropical emberizid genus. Molecular Phylogenetics and Evolution 17:367-378.

[44] MAY JH, ARGOLLO J y VEIT H (2008) Holocene landscape evolution along the Andean piedmont, Bolivian Chaco. Palaeogeography, Palaeoclimatology, Palaeoecology 260:505-520.

[45] MORENO ES, DE FREITAS LB, SPERANZA PR y SOLÍS NEFFA VG (2018) Impact of Pleistocene geoclimatic events on the genetic structure in mid-latitude South American plants: insights from the phylogeography of Turnera sidoides complex (Passifloraceae, Turneroideae). Botanical Journal of the Linnean Society 188:377-390.

[46] MORITZ C, PATTON JL, SCHNEIDER CJ y SMITH TB (2000) Diversification of Rainforest Faunas: An Integrated Molecular Approach. Annual Review of Ecology and Systematics 31:533-563.

[47] NAROSKY T y YZURIETA D (2010) Aves de Argentina y Uruguay. Vazquez Mazzini Editores, Buenos Aires.

[48] NORES M (1992) Bird speciation in subtropical South America in relation to forest expansion and retraction. Auk 109:346-357.

[49] OTTO-BLIESNER BL, MARSHALL SJ, OVERPECK JT, MILLER GH y Hu A (2006) Simulating Arctic climate warmth and icefield retreat in the last interglaciation. Science 311:1751-1753.

[50] PAILLARD D (1998) The timing of Pleistocene glaciations from a simple multiple-state climate model. Nature 391:378-381.

[51] PHILLIPS SJ, ANDERSON RP y SCHAPIRE RE (2006) Maximum entropy modeling of species geographic distributions. Ecological modelling 190:231-259.

[52] PIOVANO EL, ARIZTEGUI D, CÓRDOBA F, CIOCCALE M y SYLVESTRE F (2009) Hydrological Variability in South America Below the Tropic of Capricorn (Pampas and Patagonia, Argentina) During the Last 13.0 Ka. Pp. 323-351 en: VIMEUX F, KHODRI M y SYLVESTRE F (eds.) Past Climate Variability in South America and Surrounding Regions: from the Last Glacial Maximum to the Holocene. Springer Science and Business Media, Berlin/Heidelberg.

[53] PISIAS NG y MOORE TC (1981) The evolution of Pleistocene climate: A time series approach. Earth and Planetary Science Letters 52:450-458.

[54] PRADO DE (1993) What is the Gran Chaco vegetation in South America? I. A review. Contribution to the study of flora and vegetation of the Chaco. V. Candollea 48:145-172.

[55] PRADO LF, WAINER I, CHIESSI CM, LEDRU MP y TURCQ B (2013) A mid-Holocene climate reconstruction for eastern South America. Climate of the Past 9:2117-2133.

[56] RAMBAUT A, DRUMMOND AJ, XIE D, BAELE G y SUCHARD MA (2018) Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67:901.

[57] ROBBIATI FO, NORES MJ, ANTON AM y FORTUNATO RH (2021) Stability and fragmentation versus demographic expansion: different phylogeographic patterns in closely related sympatric legumes (Senna) from arid and semi-arid zones of mid-latitude South America. Botanical Journal of the Linnean Society 196:364-383.

[58] ROCHA AV, CABANNE GS, ALEIXO A, SILVEIRA LF, TUBARO P y CAPARROZ R (2020) Pleistocene climatic oscillations associated with landscape heterogeneity of the South American dry diagonal explains the phylogeographic structure of the narrow-billed woodcreeper (Lepidocolaptes angustirostris, Dendrocolaptidae). Journal of Avian Biology 51(09):e02537.

[59] ROZAS J, FERRER-MATA A, SÁNCHEZ-DELBARRIO JC, GUIRAO-RICO S, LIBRADO P, RAMOS-ONSINS SE y SÁNCHEZ-GRACIA A (2017) DnaSP v6: DNA Sequence Polymorphism Analysis of Large Datasets. Molecular Biology and Evolution 34:3299-3302.

[60] R DEVELOPMENT CORE TEAM (2019) R: a language and environment for statistical computing (URL: http://www.R-project.org/).

[61] SILVA JMC (1994) Can avian distribution patterns in Northern Argentina be related to retraction caused by Quaternary climatic changes? Auk 111:495-499.

[62] SILVA JMC (1996) Distribution of Amazonian and Atlantic birds in gallery forests of the Cerrado region, South America. Ornitologia Neotropical 7:1-18.

[63] SOBRAL-SOUZA T, LIMA-RIBEIRO MS y SOLFERINI VN (2015) Biogeography of Neotropical Rainforests: past connections between Amazon and Atlantic Forest detected by ecological niche modeling. Evolutionary Ecology 29:643-655.

[64] STEPHENS M y DONNELLY P (2003) A comparison of bayesian methods for haplotype reconstruction. The American Journal of Human Genetics 73:1162-1169.

[65] SYLVESTRE F (2009) Moisture Pattern During the Last Glacial Maximum in South America. Pp. 3-27 en: VIMEUX F, KHODRI M y SYLVESTRE F (eds.) Past Climate Variability in South America and Surrounding Regions: from the Last Glacial Maximum to the Holocene. Springer Science and Business Media, Berlin/Heidelberg.

[66] TAJIMA F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585-595.

[67] TRUJILLO-ARIAS N, DANTAS G, ARBELAEZ-CORTÉS E, NAOKI K, GÓMEZ MI, SANTOS FR, MIYAKI CY, ALEIXO A, TUBARO PL y CABANNE GS (2017) The niche and phylogeography of a passerine reveal the history of biological diversification between the Andean and the Atlantic forests. Molecular Phylogenetics and Evolution 112:107-121.

[68] TRUJILLO-ARIAS N, CALDERÓN L, SANTOS FR, MIYAKI CY, ALEIXO A, WITT CC, TUBARO PL y CABANNE GS (2018) Forest corridors between the central Andes and the southern Atlantic Forest enabled dispersal and peripatric diversification without niche divergence in a passerine. Molecular Phylogenetics and Evolution 128:221-232.

[69] TRUJILLO-ARIAS N, RODRÍGUEZ-CAJARVILLE MJ, SARI E, MIYAKI CY, SANTOS FR, WITT CC, BARREIRA AS, GOMEZ MI, NAOKI K, TUBARO PL y CABANNE GS (2020) Evolution between forest macrorefugia is linked to discordance between genetic and morphological variation in Neotropical passerines. Molecular Phylogenetics and Evolution 149:106849.

[70] TURCHETTO-ZOLET AC, SALGUEIRO F, TURCHETTO C, CRUZ F, VETO NM, BARROS MJF, SEGATTO ALA, FREITAS LB y MARGIS R (2016) Phylogeography and ecological niche modelling in Eugenia uniflora (Myrtaceae) suggest distinct vegetational responses to climate change between the southern and the northern Atlantic Forest. Botanical Journal of the Linnean Society 182:670-688.

[71] VUILLEUMIER BS (1971) Pleistocene Changes in the Fauna and Flora of South America. Science 173:771-780.

[72] WATANABE S, HAJIMA T, SUDO K, NAGASHIMA T, TAKEMURA T, OKAJIMA H, NOZAWA T, KAWASE H, ABE M, YOKOHATA T, ISEL T, SATO H, KATO E, TAKATA K, EMORI S y KAWAMIYA M (2011) MIROC-ESM 2010: Model description and basic results of CMIP5-20c3m experiments. Geoscientific Model Development 4:845-872.

[73] WEIR JT y SCHLUTER D (2008) Calibrating the avian molecular clock. Molecular ecology 17:2321-2328.

[74] WERNECK FP (2011) The diversification of eastern South American open vegetation biomes: Historical biogeography and perspectives. Quaternary Science Reviews 30:1630-1648.

[75] WORLDCLIM (2021) Climate Data for Modeling and GIS. URL: https://www.worldclim.org/data/index.html

[76] XIE W, LEIGH JW, YANG Q, WANG B y RAO H (2011) Bayesian inference of species divergence times using correlated quantitative characters. Evolution 65:1081-1095.

[77] YANG Z (2015) The BPP program for species tree estimation and species delimitation. Current Zoology 61:854-865.

[78] ZUCKERKANDL E y PAULING L (1965) Evolutionary divergence and convergence in proteins. Pp. 97-166 en: BRYSON V y VOGEL HJ (eds.) Evolving Genes and Proteins. Academic Press, New York.

[79] ZUCULET EA, ILSENHOUT AM y SCALABRINI A (2018) Modelos de distribución potencial para evaluar el efecto de cambios climáticos en la distribución de especies arbóreas del Bosque Atlántico. Ecología Austral 28:237-253.

[80] ZUUR AF, IENO EN, WALKER NJ, SAVELIEV AA y SMITH GM (2009) Mixed Effects Models and Extensions in Ecology with R. Springer, New York.

[81] ZUUR AF, LENO EN y ELPHICK CS (2010) A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution 1:3-14.