Abstract
It has been hypothesised that rivers serve as biogeographic barriers and Pleistocene forest refuges may explain the rich species diversity observed within Neotropical rainforests. The lack of correspondence between Amazonian and Atlantic forest species in South America is a good model for testing such hypotheses. We used molecular, ancestral area reconstruction, and potential paleodistribution analyses of Chiroxiphia pareola to test above hypotheses and examine the diversification and/or geographical expansion of populations. Six genes, two mitochondrial and four nuclear, were analysed. All population splits were estimated to have occurred in the Pliocene–Pleistocene period, and the occurrence of an Amazon population split was supported by historical river dynamics. Amazonian populations were not monophyletic, and the eastern Amazonian cluster was a sister of the Atlantic Forest population. Molecular divergence occurring between the Amazonian and Atlantic forest populations was low when compared to splits between the lineages separated by Amazonian rivers. During the early to middle Pleistocene era, regions associated with mountain slopes and riverbanks connected the Amazonian and Atlantic Forest populations near the interior of the Brazilian Northeast semiarid region, which might have facilitated species dispersal from Amazonia into the Atlantic Forest. After this point, the populations were separated, and the Atlantic Forest population remained stable until the end of the Pleistocene and Holocene eras when short-range expansion and demographic growth occurred. Our results provide evidence that highlights the role of rivers and historical climate change in the diversification of Amazonian and Atlantic Forest bird species through the Plio-Pleistocene era.
Zusammenfassung
Die Populationsgeschichte der Prachtpipra ( Chiroxiphia pareola ) unterstützt die Plio-Peistozän-Diversifizierung im Amazonasgebiet und zeigt eine junge Verbindung zum Atlantischen Wald
Es gibt die Hypothese, dass Flüsse als biogeographische Barrieren dienen und die pleistozänen Waldrückzugsgebiete möglicherweise die reiche Artenvielfalt in den neotropischen Regenwäldern erklären können. Die fehlende Übereinstimmung zwischen amazonischen und atlantischen Waldvogelarten in Südamerika bietet gute Modelle für die Prüfung solcher Hypothesen. Wir verwendeten molekulare, frühere Gebietsrekonstruktionen und mögliche Paläoverbreitungs-Analysen der Prachtpipra, um die oben erwähnte Hypothese zu testen und die Diversifizierung und/oder geographische Ausbreitung der Populationen zu prüfen. Sechs Gene, zwei mitochondriale und vier aus dem Zellkern, wurden analysiert. Dabei wurde angenommen, dass alle Aufspaltungen der Populationen im Pliozän-Pleistozän stattgefunden haben; das Auftreten einer Aufspaltung einer Amazonas-Population wurde von der historischen Fluss-Dynamik unterstützt. Die Amazonas-Populationen waren nicht monophyletisch und der östliche Amazonas-Cluster eine Schwester der Population am Atlantik. Das auf molekularer Ebene feststellbare Auseinanderlaufen der Populationen am Amazonas von denen am Atlantik war gering im Vergleich zu dem der Populationen, die durch die Amazonas-Zuflüsse voneinander getrennt sind. Während des frühen bis mittleren Pleistozäns verbanden durch Bergzüge und Flussufer miteinander verbundene Gebiete die Populationen in den Wäldern am Amazonas und am Atlantik miteinander, nahe dem Inneren der nordost-brasilianischen semiariden Regionen. Das könnte die Ausbreitung der Arten aus den amazonischen in die atlantischen Wälder erleichtert haben. Ab dann waren die Populationen voneinander getrennt; diejenige in den Wäldern am Atlantik blieb bis zum Ende des Pleistozäns und Holozäns stabil, während es zu kurzzeitiger Ausdehnung und demographischem Wachstum kam. Unsere Ergebnisse liefern Beweise für die Bedeutung von Flüssen und historischen Klimaveränderungen für die Diversifizierung der amazonischen und atlantischen Waldvogelarten während des Plio-Pleistozäns.
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References
Aleixo A (2004) Historical diversification of a Terra-firme forest Bird superspecies: a phylogeographic perspective on the role of diferente hypotheses of Amazonian diversification. Evolution (N Y) 58:1303. https://doi.org/10.1554/03-158
Aleixo A, de Rossetti DF (2007) Avian gene trees, landscape evolution, and geology: towards a modern synthesis of Amazonian historical biogeography? J Ornithol 148:443–453. https://doi.org/10.1007/s10336-007-0168-7
Andrade-lima D (1982) Present day forest refuges in Northeastern Brazil. In: Prance GT (ed) Biological diversification in the tropics. Columbia University Press, New York, New York, USA, pp 245–254
Arruda DM, Schaefer CEGR, Fonseca RS et al (2018) Vegetation cover of Brazil in the last 21 ka: new insights into the Amazonian refugia and Pleistocenic arc hypotheses. Glob Ecol Biogeogr 27:47–56. https://doi.org/10.1111/geb.12646
Auler AS, Wang X, Edwards RL et al (2004) Quarternary ecological and geomorphic changes associated with rainfall events in presently semi-arid northeastern Brazil. J Quat Sci 19:693–701. https://doi.org/10.1002/jqs.876
Auler D, Teixeira Dalmolin A, Santos Fenalti V (2009) Abordagem Temática: natureza dos temas em Freire e no enfoque CTS. Alexandria Rev Educ Ciência Tecnol 2:67–84 (10.5007/%x)
Ayres JM, Clutton-Brock TH (1992) River boundaries and species range size in amazonian primates. Am Nat 140:531–537. https://doi.org/10.1086/285427
Bandelt HJ, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48. https://doi.org/10.1093/oxfordjournals.molbev.a026036
Batalha-Filho H, Fjeldså J, Fabre PH, Miyaki CY (2013) Verbindungen zwischen atlantischen und amazonischen Waldvogelfaunen spiegeln distinkte historische Ereignisse wider. J Ornithol 154:41–50. https://doi.org/10.1007/s10336-012-0866-7
Batalha-Filho H, Pessoa RO, Fabre P-H et al (2014) Phylogeny and historical biogeography of gnateaters (Passeriformes, Conopophagidae) in the South America forests. Mol Phylogenet Evol 79:422–432. https://doi.org/10.1016/j.ympev.2014.06.025
Bates JM, Hackett SJ, Cracraft J (1998) Area-relationships in the Neotropical lowlands: an hypothesis based on raw distributions of Passerine birds. J Biogeogr 25:783–793. https://doi.org/10.1046/j.1365-2699.1998.2540783.x
Behling H (2002) Carbon storage increases by major forest ecosystems in tropical South America since the Last Glacial Maximum and the early Holocene. Glob Planet Change 33:107–116. https://doi.org/10.1016/S0921-8181(02)00065-6
Berv JS, Prum RO (2014) A comprehensive multilocus phylogeny of the Neotropical cotingas (Cotingidae, Aves) with a comparative evolutionary analysis of breeding system and plumage dimorphism and a revised phylogenetic classification. Mol Phylogenet Evol 81:120–136. https://doi.org/10.1016/j.ympev.2014.09.001
Brown KS Jr, Ab’Saber AN (1979) Ice-age forest refuges and evolution in the neotropics: correlation of paleoclimatological, geomorphological and pedological data with modern biological endemism. Paleoclimas 5:1–30
Brown JL, Hill DJ, Dolan AM et al (2018) PaleoClim, high spatial resolution paleoclimate surfaces for global land areas. Sci Data 5:180254. https://doi.org/10.1038/sdata.2018.254
Bruen TC, Philippe H, Bryant D (2006) A simple and robust statistical test for detecting the presence of recombination. Genetics 172:2665–2681. https://doi.org/10.1534/genetics.105.048975
Brumfield RT (2012) Inferring the origins of lowland Neotropical birds. Auk 129:367–376. https://doi.org/10.1525/auk.2012.129.3.367
Cabanne G, d’Horta F, Sari E et al (2008) Nuclear and mitochondrial phylogeography of the Atlantic forest endemic Xiphorhynchus fuscus (Aves: Dendrocolaptidae): Biogeography and systematics implications. Mol Phylogenet Evol 49:760–773. https://doi.org/10.1016/j.ympev.2008.09.013
Campbell KE, Frailey CD, Romero-Pittman L (2006) The pan-Amazonian Ucayali Peneplain, late Neogene sedimentation in Amazonia, and the birth of the modern amazon river system. Palaeogeogr Palaeoclimatol Palaeoecol 239:166–219. https://doi.org/10.1016/j.palaeo.2006.01.020
Capurucho JMG, Ashley MV, Ribas CC, Bates JM (2018) Connecting Amazonian, Cerrado, and Atlantic forest histories: paraphyly, old divergences, and modern population dynamics in tyrant-manakins (Neopelma/Tyranneutes, aves: pipridae). Mol Phylogenet Evol 127:696–705. https://doi.org/10.1016/j.ympev.2018.06.015
Carnaval AC, Moritz C (2008) Historical climate modelling predicts patterns of current biodiversity in the Brazilian Atlantic forest. J Biogeogr 35:1187–1201. https://doi.org/10.1111/j.1365-2699.2007.01870.x
Carnaval AC, Hickerson MJ, Haddad CFB et al (2009) Stability predicts genetic diversity in the Brazilian Atlantic forest hotspot. Science 80-(323):785–789. https://doi.org/10.1126/science.1166955
CarvalhoDe CS, Nascimento Do NFF, De Araujo HFP (2017) Bird distributional patterns support biogeographical histories and are associated with bioclimatic units in the Atlantic Forest. Brazil. Zootaxa 4337:223. https://doi.org/10.11646/zootaxa.4337.2.3
Castro-Astor IN (2014) Phylogeographic study of two neotropical bird species, the red-headed manakin (Pipna Rubrocapilla) and the white-crowned manakin (Dixiphia Pipra). Academic Works, Thesis. The City College of New York, 160 Convent Ave., New York, NY 10031. https://academicworks.cuny.edu/cc_etds_theses/217
Cerqueira PV, Santos MPD, Aleixo A (2016) Phylogeography, inter-specific limits and diversification of Turdus ignobilis (Aves: Turdidae). Mol Phylogenet Evol 97:177–186. https://doi.org/10.1016/j.ympev.2016.01.005
Cheng H, Sinha A, Cruz FW et al (2013) Climate change patterns in Amazonia and biodiversity. Nat Commun 4:1411. https://doi.org/10.1038/ncomms2415
Costa LP (2003) The historical bridge between the Amazon and the Atlantic Forest of Brazil: a study of molecular phylogeography with small mammals. J Biogeogr 30:71–86. https://doi.org/10.1046/j.1365-2699.2003.00792.x
Costa GC, Hampe A, Ledru M-P et al (2018) Biome stability in South America over the last 30 kyr: Inferences from long-term vegetation dynamics and habitat modelling. Glob Ecol Biogeogr 27:285–297. https://doi.org/10.1111/geb.12694
Cracraft J, Prum RO (1988) Patterns and processes of diversification: speciation and historical congruence in some Neotropical birds. Evolution (NY) 42:603–620. https://doi.org/10.1111/j.1558-5646.1988.tb04164.x
de Rossetti DF, de Toledo PM, Góes AM (2005) New geological framework for Western Amazonia (Brazil) and implications for biogeography and evolution. Quat Res 63:78–89. https://doi.org/10.1016/j.yqres.2004.10.001
Dhorta F, Cabanne G, Meyer D, Miyaki C (2011) The genetic effects of late quaternary climatic changes over a tropical latitudinal gradient: diversification of an Atlantic Forest passerine. Mol Ecol 20:1923–1935. https://doi.org/10.1111/j.1365-294X.2011.05063.x
Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:1–8. https://doi.org/10.1186/1471-2148-7-214
Elith J, Phillips SJ, Hastie T et al (2011) A statistical explanation of MaxEnt for ecologists. Divers Distrib 17:43–57. https://doi.org/10.1111/j.1472-4642.2010.00725.x
Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinforma 1:117693430500100. https://doi.org/10.1177/117693430500100003
Friesen VL, Congdon BC, Walsh HE, Birt TP (1997) Intron variation in marbled murrelets detected using analyses of single-stranded conformational polymorphisms. Mol Ecol 6:1047–1058. https://doi.org/10.1046/j.1365-294X.1997.00277.x
Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925
Haffer J (1969) Speciation in Amazonian Forest Birds. Science 80-(165):131–137. https://doi.org/10.1126/science.165.3889.131
Haffer J (1987) Biogeography of Neotropical birds. In: Whitmore TC, Prance GT (eds) Biogeography and Quaternary History of Tropical America. Clarendon Press, Oxford, pp 105–150
Haffer J (1997) Alternative models of vertebrate speciation in Amazonia: an overview. Biodivers Conserv 6:451–476. https://doi.org/10.1023/A:1018320925954
Heled J, Drummond AJ (2008) Bayesian inference of population size history from multiple loci. BMC Evol Biol 8:1–15. https://doi.org/10.1186/1471-2148-8-289
Heled J, Drummond AJ (2010) Bayesian inference of species trees from multilocus data. Mol Biol Evol 27:570–580. https://doi.org/10.1093/molbev/msp274
Higgins D, Thompson J, Gibson T et al (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680. https://doi.org/10.1093/nar/22.22.4673
Hijmans RJ, Cameron SE, Parra JL et al (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978. https://doi.org/10.1002/joc.1276
Ho SYW, Shapiro B (2011) Skyline-plot methods for estimating demographic history from nucleotide sequences. Mol Ecol Resour 11:423–434. https://doi.org/10.1111/j.1755-0998.2011.02988.x
Hoorn C, Wesselingh FP, ter Steege H et al (2010) Amazonia through time: andean uplift, climate change, landscape evolution, and biodiversity. Science 80-(330):927–931. https://doi.org/10.1126/science.1194585
Huang W, Fu YX, Chang BH et al (1998) Sequence variation in ZFX introns in human populations. Mol Biol Evol 15:138–142. https://doi.org/10.1093/oxfordjournals.molbev.a025910
Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755. https://doi.org/10.1093/bioinformatics/17.8.754
Hughes CE, Pennington RT, Antonelli A (2013) Neotropical plant evolution: assembling the big picture. Bot J Linn Soc 171:1–18. https://doi.org/10.1111/boj.12006
Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267. https://doi.org/10.1093/molbev/msj030
Ingenloff K, Peterson AT (2015) Trans-Amazon dispersal potential for Crotalus durissus during Pleistocene climate events. Biota Neotrop. https://doi.org/10.1590/1676-06032015008113
Ivanova NV, Zemlak TS, Hanner RH, Hebert PDN (2007) Universal primer cocktails for fish DNA barcoding. Mol Ecol Notes 7:544–548. https://doi.org/10.1111/j.1471-8286.2007.01748.x
Kirwan G, Green G (2011) Cotingas and Manakins. Princeton University Press, Reprint
Latrubesse EM, Cozzuol M, da Silva-Caminha SAF et al (2010) The late miocene paleogeography of the amazon basin and the evolution of the Amazon river system. Earth-Science Rev 99:99–124. https://doi.org/10.1016/j.earscirev.2010.02.005
Ledo RMD, Colli GR (2017) The historical connections between the Amazon and the Atlantic Forest revisited. J Biogeogr 44:2551–2563. https://doi.org/10.1111/jbi.13049
Leite YLR, Costa LP, Loss AC et al (2016) Neotropical forest expansion during the last glacial period challenges refuge hypothesis. Proc Natl Acad Sci USA 113:1008–1013. https://doi.org/10.1073/pnas.1513062113
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. https://doi.org/10.1093/bioinformatics/btp187
Lovette IJ (2004) Mitochondrial dating and mixed support for the “2% rule” in birds. Auk 121:1–6. https://doi.org/10.1093/auk/121.1.1
Maldonado-Coelho M (2012) Climatic oscillations shape the phylogeographical structure of Atlantic Forest fire-eye antbirds (Aves: Thamnophilidae). Biol J Linn Soc 105:900–924. https://doi.org/10.1111/j.1095-8312.2011.01823.x
Matzke NJ (2018) BioGeoBEARS: BioGeografia com Análise Evolutiva Bayesiana (e probabilidade) com R Scripts. versão 1.1.1, publicada no GitHub em 6 de novembro de 2018. https://doi.org/10.5281/zenodo.1478250
Miller WD (1908) A review of the manakins of the genus Chiroxiphia. Bull Am Museum Nat Hist 24:331–347
Nei M (1987) Molecular evolutionary genetics. Columbia University Press, reimpressão, p 512, ISBN 0231063210, 9780231063210
Oliveira PE, Barreto AMF, Suguio K (1999) Late Pleistocene/Holocene climatic and vegetational history of the Brazilian caatinga: the fossil dunes of the middle São Francisco River. Palaeogeogr Palaeoclimatol Palaeoecol 152:319–337. https://doi.org/10.1016/S0031-0182(99)00061-9
Ortiz-Jaureguizar E, Cladera GA (2006) Paleoenvironmental evolution of southern South America during the Cenozoic. J Arid Environ 66:498–532. https://doi.org/10.1016/j.jaridenv.2006.01.007
Pennington TR, Lewis G, Ratter J (2006) An overview of the plant diversity, biogeography and conservation of neotropical savannas and seasonally dry forests. Syst Assoc Spec Vol 1–29. https://doi.org/10.1201/9781420004496.ch1
Phillips SJ, Dudík M, Schapire RE (2004) A maximum entropy approach to species distribution modeling. In: Twenty-first international conference on Machine learning - ICML ’04. ACM Press, New York, USA, p 83. http://portal.acm.org/citation.cfm?doid=1015330.1015412
Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Modell 190:231–259. https://doi.org/10.1016/j.ecolmodel.2005.03.026
Prates I, Rivera D, Rodrigues MT, Carnaval AC (2016) A mid-Pleistocene rainforest corridor enabled synchronous invasions of the Atlantic Forest by Amazonian anole lizards. Mol Ecol 25:5174–5186. https://doi.org/10.1111/mec.13821
Primmer CR, Borge T, Lindell J, Saetre G-P (2002) Single-nucleotide polymorphism characterization in species with limited available sequence information: high nucleotide diversity revealed in the avian genome. Mol Ecol 11:603–612. https://doi.org/10.1046/j.0962-1083.2001.01452.x
Pybus OG, Rambaut A, Harvey PH (2000) An integrated framework for the inference of viral population history from reconstructed genealogies. Genetics 155:1429–1437
Ramos-Onsins SE, Rozas J (2002) Statistical Properties of New Neutrality Tests Against Population Growth. Mol Biol Evol 19:2092–2100. https://doi.org/10.1093/oxfordjournals.molbev.a004034
Ree RH, Moore BR, Webb CO, Donoghue MJ (2005) A likelihood framework for inferring the evolution of geographic range on phylogenetic trees. Evolution (NY) 59:2299–2311. https://doi.org/10.1111/j.0014-3820.2005.tb00940.x
Ribas CC, Aleixo A, Nogueira ACR et al (2012) A palaeobiogeographic model for biotic diversification within Amazonia over the past three million years. Proc R Soc B Biol Sci 279:681–689. https://doi.org/10.1098/rspb.2011.1120
Ribas CC, Maldonado-Coelho M, Smith BT et al (2012) Towards an integrated historical biogeography of the Neotropical Lowland Avifauna: combining Diversification analysis and Landscape Evolution. Ornitol Neotrop 23:187–206
Ridgely RS, Tudor G (1994) The Birds of South America, 1st edn. University of Texas Press, Austin
Rocha TC, Sequeira F, Aleixo A et al (2015) Molecular phylogeny and diversification of a widespread Neotropical rainforest bird group: the Buff-throated Woodcreeper complex, Xiphorhynchus guttatus/susurrans (Aves: Dendrocolaptidae). Mol Phylogenet Evol 85:131–140. https://doi.org/10.1016/j.ympev.2015.02.004
Ronquist F (1997) Dispersal-vicariance analysis: a new approach to the quantification of historical biogeography. Syst Biol 46:195–203. https://doi.org/10.1093/sysbio/46.1.195
Roos AL, de Souza EA, de Campos CB et al (2012) Primeiro registro documentado do jacu-estalo neomorphus geoffroyi temminck, 1820 para o bioma caatinga. Rev Bras Ornitol 20:81–85
Santos AM, Cavalcanti DR, da Silva JMC, Tabarelli M (2007) Biogeographical relationships among tropical forests in north-eastern Brazil. J Biogeogr 34:437–446. https://doi.org/10.1111/j.1365-2699.2006.01604.x
Sick H (1997) Ornitologia Brasileira. Editora Universidade De Brasilia, Rio de Janeiro
Silva JMC, Garda AA (2010) Padrões e processos Biogeográficos na Amazônia. In: Carvalho CJBC, Almeida EAB (eds) Biogeografia Da America Do Sul Padroes E Processos, 1st edn. Roca. pp 189–197. ISBN: 8572418962
Silva SM, Agne CE, Aleixo A, Bonatto SL (2018) Phylogeny and systematics of Chiroxiphia and Antilophia manakins (Aves, Pipridae). Mol Phylogenet Evol 127:706–711. https://doi.org/10.1016/j.ympev.2018.06.016
Silveira MHB, Mascarenhas R, Cardoso D, Batalha-Filho H (2019) Pleistocene climatic instability drove the historical distribution of forest islands in the northeastern Brazilian Atlantic Forest. Palaeogeogr Palaeoclimatol Palaeoecol 527:67–76. https://doi.org/10.1016/j.palaeo.2019.04.028
Snow D (2020) Blue-backed Manakin (Chiroxiphia pareola), version 1.0. In: del Hoyo J, Elliott A, Sargatal J, Christie DA, de Juana E (eds) Birds of the World. Cornell Lab of Ornithology, Ithaca, NY, USA. https://doi.org/10.2173/bow.blbman1.01
Sobral-Souza T, Lima-Ribeiro MS (2017) De volta ao passado: revisitando a história biogeográfica das florestas neotropicais úmidas. Oecologia Aust 21:93–107. https://doi.org/10.4257/oeco.2017.2102.01
Sorenson M (2003) Avian mtDNA primers. Boston University, pp 1–7. http://people.bu.edu/MSOREN/Bird.mt.Primers.pdf
Sorenson MD, Ast JC, Dimcheff DE et al (1999) Primers for a PCR-based approach to mitochondrial genome sequencing in birds and other vertebrates. Mol Phylogenet Evol 12:105–114. https://doi.org/10.1006/mpev.1998.0602
Sousa-Neves T, Aleixo A, Sequeira F (2013) Cryptic patterns of diversification of a widespread Amazonian Woodcreeper species complex (Aves: Dendrocolaptidae) inferred from multilocus phylogenetic analysis: Implications for historical biogeography and taxonomy. Mol Phylogenet Evol 68:410–424. https://doi.org/10.1016/j.ympev.2013.04.018
Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989. https://doi.org/10.1086/319501
Tajima F (1989) The effect of change in population size on DNA polymorphism. Genetics 123:597–601
Tamura K, Peterson D, Peterson N et al (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. https://doi.org/10.1093/molbev/msr121
Team RC (2013) R-a language and environment for statistical computing. R Foundation for statistical computing, Vienna. ISBN 3-900051-07-0
Terribile L, Diniz-Filho J, Jr De Marco P (2010) How many studies are necessary to compare niche-based models for geographic distributions? Inductive reasoning may fail at the end. Brazilian J Biol 70:263–269. https://doi.org/10.1590/S1519-69842010000200005
Thom G, Aleixo A (2015) Cryptic speciation in the white-shouldered antshrike (Thamnophilus aethiops, Aves: Thamnophilidae): the tale of a transcontinental radiation across rivers in lowland Amazonia and the northeastern Atlantic Forest. Mol Phylogenet Evol 82:95–110. https://doi.org/10.1016/j.ympev.2014.09.023
Traylor MA Jr, Fitzpatrick JW (1982) A survey of tyrant flycatchers. The livingbirds 19:7–50
Vanzolini PE, Williams EE (1970) South american anoles: the geographic differentiation and evolution of the anolis Chrysolepis species group (Sauria, Iguanidae). Arq Zool 19:125. https://doi.org/10.11606/issn.2176-7793.v19i3-4p125-298
Wallace AR (1852) On the monkeys of the Amazon. Proc Zool Soc Lond 451–454. https://doi.org/10.1080/037454809494374
Wallace AR (1854) On the Monkeys of the Amazon. Ann Mag Nat Hist 14:451–454. https://doi.org/10.1080/037454809494374
Wang X, Auler AS, Edwards LL et al (2004) Wet periods in northeastern Brazil over the past 210 kyr linked to distant climate anomalies. Nature 432:740–743. https://doi.org/10.1038/nature03067
Webb SD, Opdyke ND (1995) Global climatic influences on Cenozoic land mammal faunas. Effects of Past Global Change on Life. National Academies Press, Washington, pp 184–208
Webb SD, Rancy A (1996) Late Cenozoic evolution of the Neotropical mammal fauna. In: Jackson JBC, Budd AF, Coates AG (eds) Evolution and Environments in Tropical Americas. The University of Chicago Press, Chicago, pp 335–358
Weir JT, Schluter D (2008) Calibrating the avian molecular clock. Mol Ecol 17:2321–2328. https://doi.org/10.1111/j.1365-294X.2008.03742.x
Werneck FP (2011) The diversification of eastern South American open vegetation biomes: historical biogeography and perspectives. Quat Sci Rev 30:1630–1648. https://doi.org/10.1016/j.quascirev.2011.03.009
Werneck FP, Gamble T, Colli GR et al (2012) Deep diversification and long-term persistence in the south american ´dry diagonal´: integrating continent-wide phylogeography and distribution modeling of geckos. Evolution (NY) 66:3014–3034. https://doi.org/10.1111/j.1558-5646.2012.01682.x
Whitmore TC, Prance GT (1987) Biogeography and quaternary history in tropical America. Oxford University Press, p 224. ISBN: 0198545460. https://www.cambridge.org/core/product/identifier/S0016756800023645/type/journal_article
Willis EO (1992) Zoogeographical origins of eastern Brazilian. Ornitol Neotrop 3:1–15. https://doi.org/10.1002/mmnd.4800250112
Young N, Carter L, Evangelista P (2011) A MaxEnt Model v3.3.3e Tutorial (ArcGIS v10). ACM Press, New York, USA, p 1–30. https://doi.org/10.1145/1015330.1015412
Acknowledgements
We are grateful to the anonymous reviewer and Alexandre Aleixo for their comments and suggestions on the manuscript. The authors thank the Rede de Plataformas Tecnológicas for use of its Sequencing facility in Instituto Gonçalo Moniz (FIOCRUZ)—Bahia. Nayla F. F. Nascimento thanks Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for scholarship. Henrique Batalha-Filho thanks Fundação de Amparo à Pesquisa do Estado da Bahia (FAPESB)—RED0045/2014; JCB0026/2016, Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)—443249/2014-8 and Pró-Reitoria de Pesquisa, Criação e Inovação/Universidade Federal da Bahia (PROPCI/UFBA)—PRODOC-2013/5813 for funding. All biological material used in the research came from scientific collections.
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Supplementary file2 (PDF 259 KB) ESM_2 On vertebrates endemism areas: A) Rondônia, B) Inambari, C) Napo, D) Imeri, E) Guiana, F) Tapajós, G) Xingu, H) Belém, I) Brejos de altitude – Ibiapaba (Ceará), and J) Atlantic Forest
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do Nascimento, N.F.F., Agne, C.E.Q., Batalha-Filho, H. et al. Population history of the Blue-backed Manakin (Chiroxiphia pareola) supports Plio-Pleistocene diversification in the Amazon and shows a recent connection with the Atlantic Forest. J Ornithol 162, 549–563 (2021). https://doi.org/10.1007/s10336-020-01845-x
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DOI: https://doi.org/10.1007/s10336-020-01845-x