Evolutionary Ecology

, Volume 33, Issue 1, pp 111–148 | Cite as

Integrating phylogeography and ecological niche modelling to test diversification hypotheses using a Neotropical rodent

  • Arielli Fabrício MachadoEmail author
  • Mário Silva Nunes
  • Cláudia Regina Silva
  • Marcelo Augusto dos SantosJr.
  • Izeni Pires Farias
  • Maria Nazareth Ferreira da Silva
  • Marina Anciães
Original Paper


Several hypotheses have been used to explain diversification in the Neotropics. Integrating evolution with ecology extends the scope of testing the frameworks of these hypotheses. We test diversification hypotheses by integrating phylogeography and ecological niche models (ENMs) using the rodent Hylaeamys megacephalus (Azara’s broad-headed oryzomys or large headed rice rat) of the Amazon and dry forests, as a model. We estimated divergence times, ancestral areas, diversification events, historical demography, haplotype sharing, and genetic distances based on the mitochondrial cytochrome b gene. We generated ENMs and tested for niche divergence between lineages; integrated genetic data to predict gene flow corridors; and projected paleodistributions for comparison with historical demography. We found high structuring in northern Amazonia on the left bank of the Amazon River, and less structure but secondary contact in southern Amazonia and dry forests. The Northern Amazonian lineage diverged from the other lineages through dispersal followed by vicariance due to the Amazon River about 1.35 Mya, while the Southern Amazonian and Cerrado lineages diverged through dispersal about 0.78 Mya. Paleodistribution models revealed expansions of dry forest lineages consistent with the Refugia Hypothesis, but not retraction for the humid forest lineage, which were not congruent with historical demography data. Niche divergence was not supported for the Northern Amazonian lineage, whereas habitat corridors linking current lineages suggest environmental continuity to their distributions that is concordant with a riverine barrier. In contrast, niche divergence was supported between the Southern Amazonian and Cerrado lineages, indicating that isolation followed by ecological divergence likely acted on this diversification. The recent Amazon River barrier and ecological differentiation observed here will surely provide insight for future studies and hypotheses of biodiversity diversification in the Neotropics. Studies that integrate evolution and ecology promise to disentangle alternative hypotheses and shed light on the biogeography of this megadiverse region.


Biogeography Amazon River Neotropical rodent Riverine barrier Refugia Ecological speciation Niche conservatism 



We thank A. Townsend Peterson, Fernanda P. Werneck, Rafael N. Leite and Igor L. Kaeffer for help in delineating the project; Rafael N. Leite and Rogério Rossi for providing tissue samples; Cleuton L. Miranda for reviewing the manuscript and William T. Peçanha for help with phylogenetic analyses. We also thank the team from LEGAL for helping with molecular sampling and analyses, and Camila D. Ritter, Cristiane F. Marks and Tomas Hrbek for help with phylogenetic analyses and for reviewing this manuscript. Thanks got to Glenn H. Shepard and Erik Wild for helping with the English language. This research was supported by CNPq/FAPEAM/SISBIOTA (Rede BioPHAM) 563348/2010 to IPF and MNFS. This study is part of AFM’s Master’s thesis in the ecology graduate program of INPA, and was supported by a fellowship from CNPq. The authors declare no conflicts of interest.

Supplementary material

10682_2019_9968_MOESM1_ESM.docx (14 kb)
S1. Laboratory techniques used for amplification of mitochondrial cytochrome b gene sequence fragments. (DOCX 15 kb)
10682_2019_9968_MOESM2_ESM.xlsx (16 kb)
Table S2. Occurrence records for Hylaeamys megacephalus used for producing the ecological niche model (ENM) for the entire species. ID = identification number. The records with identification number 66, 68, 69, 90, 92 102, 104, 113 and 114 were added for the ENM of the Southern Amazonian lineage (black dots in Fig. 1). (XLSX 16 kb)


  1. Aide TM, Rivera E (1998) Geographic patterns of genetic diversity in Poulsenia armata (Moraceae): implications for the theory of Pleistocene refugia and the importance of riparian forest. J Biogeogr 25(4):695–705Google Scholar
  2. Alfaro JWL, Boubli JP, Paim FP, Ribas CC, da Silva MNF, Messias MR, Pinho GM (2015) Biogeography of squirrel monkeys (genus Saimiri): South-central Amazon origin and rapid pan-Amazonian diversification of a lowland primate. Mol Phylogenet Evol 82:436–454Google Scholar
  3. Alvarado-Serrano DF, Knowles LL (2014) Ecological niche models in phylogeographic studies: applications, advances and precautions. Mol Ecol Resour 14:233–248Google Scholar
  4. Amman BR, Hanson JD, Longhofer LK, Hoofer SR, Bradley RD (2006) Intron 2 (Adh1-I2) of the alcohol dehydrogenase gene: a potential nuclear DNA phylogenetic marker for mammals. Occas Pap Mus Texas Tech Univ 256:1–16Google Scholar
  5. Anderson RP, Raza A (2010) The effect of the extent of the study region on GIS models of species geographic distributions and estimates of niche evolution: preliminary tests with montane rodents (genus Nephelomys) in Venezuela. J Biogeogr 37:1378–1393Google Scholar
  6. Antonelli A, Quijada-Mascareñas A, Crawford AJ, Bates JM, Velazco PM, Wüster W (2010) Molecular studies and phylogeography of Amazonian tetrapods and their relation to geological and climatic models. Amazon Landsc Species Evol Look Past. Google Scholar
  7. Avise JC (1994) Molecular markers, natural history, and evolution. Chapman & Hall, New YorkGoogle Scholar
  8. Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge. ISBN 9780674666382Google Scholar
  9. Ayers JM, Clutton-Brock TH (1992) River boundaries and species range size in Amazonian primates. Am Nat 140(3):531–537Google Scholar
  10. Barrett JC, Fry B, Maller JDMJ, Daly MJ (2005) Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21(2):263–265Google Scholar
  11. Bartoleti LFDM, Peres EA, Sobral-Souza T, Fontes FVHM, Silva MJD, Solferini VN (2017) Phylogeography of the dry vegetation endemic species Nephila sexpunctata (Araneae: Araneidae) suggests recent expansion of the Neotropical dry diagonal. J Biogeogr 44(9):2007–2020Google Scholar
  12. Bates JM (2000) Allozymic genetic structure and natural habitat fragmentation: data for five species of Amazonian forest birds. Condor 1:770–783Google Scholar
  13. Bates JM (2002) The genetic effects of forest fragmentation on five species of Amazonian birds. J Avian Biol 33(3):276–294Google Scholar
  14. Bergallo HG, Magnusson WE (2004) Factors affecting the use of space by two rodent species in Brazilian Atlantic forest. Mammalia 68(2–3):121–132Google Scholar
  15. Bonaccorso E, Koch I, Peterson AT (2006) Pleistocene fragmentation of Amazon species’ ranges. Divers Distrib 12(2):157–164Google Scholar
  16. Borges SH, Da Silva JMC (2012) A new area of endemism for Amazonian birds in the Rio Negro Basin. Wilson J Ornithol 124(1):15–23Google Scholar
  17. Boria RA, Olson LE, Goodman SM, Anderson RP (2014) Spatial filtering to reduce sampling bias can improve the performance of ecological niche models. Ecol Model 275:73–77. Google Scholar
  18. Boubli JP, Ribas C, Lynch Alfaro JW, Alfaro ME, da Silva MNF, Pinho GM, Farias IP (2014) Spatial and temporal patterns of diversification on the Amazon: a test of the riverine hypothesis for all diurnal primates of Rio Negro and Rio Branco in Brazil. Mol Phylogenet Evol 82:400–412Google Scholar
  19. Bradley RD, Baker RJ (2001) A test of the genetic species concept: cytochrome-b sequences and mammals. J Mammal 82(4):960–973Google Scholar
  20. Brown JL (2014) SDMtoolbox: a python-based GIS toolkit for landscape genetic, biogeographic and species distribution model analyses. Methods Ecol Evol 5(7):694–700Google Scholar
  21. Cáceres NC (2007) Semideciduous Atlantic Forest mammals and the role of the Paraná River as a riverine barrier. Neotrop Biol Conserv 2(2):84–89Google Scholar
  22. Calenge C (2011) Home range estimation in R: the adehabitatHR package. Office national de la classe et de la faune sauvage, Saint Benoist, AuffargisGoogle Scholar
  23. Campbell KE Jr, Frailey CD, Romero-Pittman L (2006) The Pan-Amazonian Ucayali Peneplain, late Neogenese dimentation in Amazonia, and the birth of the modern Amazon River system. Palaeogeogr Palaeoclimatol Palaeoecol 239:166–219Google Scholar
  24. Carnaval AC, Hickerson MJ, Haddad CF, Rodrigues MT, Moritz C (2009) Stability predicts genetic diversity in the Brazilian Atlantic forest hotspot. Science 323(5915):785–789Google Scholar
  25. Chan LM, Brown JL, Yoder AD (2011) Integrating statistical genetic and geospatial methods brings new power to phylogeography. Mol Phylogenet Evol 59:523–537Google Scholar
  26. 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 30:71–86Google Scholar
  27. Cox BC, Moore PD (2005) Biogeography: an ecological and evolutionary approach, 7th edn. Blackwell Publishing, LondonGoogle Scholar
  28. Cracraft J (1985) Historical biogeography and patterns of differentiation within the South American avifauna: areas of endemism. Ornithol Monogr 36:49–84Google Scholar
  29. Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295Google Scholar
  30. Da Silva MNF, Patton JL (1993) Amazonian phylogeography: mtDNA sequence variation in arboreal echimyid rodents (Caviomorpha). Mol Phylogenet Evol 2:243–255Google Scholar
  31. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9(8):772Google Scholar
  32. D’Elı́a G (2003) Phylogenetics of Sigmodontinae (Rodentia, Muroidea, Cricetidae), with special reference to the akodont group, and with additional comments on historical biogeography. Cladistics 19(4):307–323Google Scholar
  33. Drummond AJ, Nicholls GK, Rodrigo AG, Solomon W (2002) Estimating mutation parameters, population history and genealogy simultaneously from temporally spaced sequence data. Genetics 161:1307–1320Google Scholar
  34. Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973Google Scholar
  35. Elith J, Kearney M, Phillips SJ (2010) The art of modelling range-shifting species. Methods Ecol Evol 1:330–342Google Scholar
  36. Elith J, Phillips SJ, Hastie T, Dudík M, Chee YE, Yates CJ (2011) A statistical explanation of MaxEnt for ecologists. Divers Distrib 17:43–57Google Scholar
  37. Emmons LH, Patton JL (2005) A new species of Oryzomys (Rodentia: Muridae) from eastern Bolivia. Am Mus Novitates 18(3478):1–28Google Scholar
  38. Endler JA (1977) Geographic variation, speciation, and clines (No. 10). Princeton University Press, PrincetonGoogle Scholar
  39. Endler JA (1982) Problems in distinguishing historical from ecological factors in biogeography. Am Zool 22(2):441–452Google Scholar
  40. Ersts PJ (2015) Geographic distance matrix generator (version 1.2.3). American Museum of Natural History, Center for Biodiversity and Conservation. Accessed 20 May 2015
  41. Farias MB, Oliveira JA, Bonvicino RC (2013) Filogeografia de populações brasileiras de Marmosa (Marmosa) murina (Didelphimorphia, Didelphidae). Rev Nordestina Biol 21(2):27–52Google Scholar
  42. Fernandes AM, Wink M, Sardelli C, Aleixo A (2014) Multiple speciation across the Andes and throughout Amazonia: the case of the spot-backed antbird species complex (Hylophylax naevius/Hylophylax naevioides). J Biogeogr 41(6):1094–1104Google Scholar
  43. Fine PVA, Daly DC, Muñoz GV, Mesones I, Cameron KM (2005) The contribution of edaphic heterogeneity to the evolution and diversity of Burseraceae trees in the western Amazon. Evolution 59(7):1464–1478Google Scholar
  44. Fraser DJ, Bernatchez L (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Mol Ecol 10:2741–2752Google Scholar
  45. Frey JK (1993) Modes of peripheral isolate formation and speciation. Syst Biol 42(3):373–381Google Scholar
  46. Funk WC, Caldwell JP, Peden CE, Padial JM, De la Riva I et al (2007) Tests of biogeographic hypotheses for diversification in the Amazonian forest frog, Physalaemus petersi. Mol Phylogenet Evol 44:825–837Google Scholar
  47. Galtier N, Nabholz B, Glémin S, Hurst GD (2009) Mitochondrial DNA as a marker of molecular diversity: a reappraisal. Mol Ecol 18(22):4541–4550Google Scholar
  48. Garzón-Orduña IJ, Benetti-Longhini JE, Brower AVZ (2014) Timing the diversification of the Amazonian biota: butterfly divergences are consistent with Pleistocene refugia. J Biogeogr 41:1631–1638Google Scholar
  49. Gascon C, Malcolm JR, Patton JL, da Silva MNF, Bogart JP, Lougheed SC, Peres CA, Neckel S, Boag PT (2000) Riverine barriers and the geographic distribution of Amazonian species. Proc Natl Acad Sci 97(25):13672–13677Google Scholar
  50. Godoy LP (2015) Pequenos mamíferos não voadores (Mammalia: Didelphimorphia e Rodentia) do baixo rio Xingu. Dissertation, Escola Superior de Agricultura “Luiz de Queiroz”, Centro de Energia Nuclear na Agricultura. Available from Accessed Nov 2016
  51. Haffer J (1969) Speciation in Amazonian forest birds. Science 165:131–137Google Scholar
  52. Haffer J, Prance GT (2001) Climatic forcing of evolution in Amazonia during the Cenozoic: on the refuge theory of biotic differentiation. Amazoniana 16(3):579–607Google Scholar
  53. Hall JPW, Harvey DJ (2002) The phylogeography of Amazonia revisited: new evidence from riodinid butterflies. Evolution 56:1489–1497Google Scholar
  54. Hansen J, Sato M, Russell G, Kharecha P (2013) Climate sensitivity, sea level and atmospheric carbon dioxide. Philos Trans R Soc A 371(2001):20120294. Google Scholar
  55. Hanson JD (2008) Molecular phylogenetics of the tribe Oryzomyini: does a multi-gene approach help resolve a systematic conundrum. Doctor of Philosophy Thesis, Texas Tech UniversityGoogle Scholar
  56. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978Google Scholar
  57. Hijmans RJ, Phillips S, Leathwick J, Elith J, Hijmans MRJ (2017) Package ‘dismo’. Circles 9(1):1–68Google Scholar
  58. Hoorn C, Wesselingh FP, Ter Steege H, Bermudez MA, Mora A, Sevink J, Jaramillo C (2010) Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity. Science 330(6006):927–931Google Scholar
  59. Hoorn C, Bogotá-A GR, Romero-Baez M, Lammertsma EI, Flantua SGA, Dantas EL, Dino R, do Carmo DA, Chemale F Jr (2017) The Amazon at sea: onset and stages of the Amazon River from a marine record, with special reference to Neogene plant turnover in the drainage basin. Glob Planet Change 153:51–65Google Scholar
  60. Hubbell SP (2001) The unified neutral theory of biodiversity and biogeography. Princeton University Press, Princeton. ISBN 9780691021287Google Scholar
  61. Hurst GD, Jiggins FM (2005) Problems with mitochondrial DNA as a marker in population, phylogeographic and phylogenetic studies: the effects of inherited symbionts. Proc R Soc B Biol Sci 272(1572):1525–1534Google Scholar
  62. Hutchinson GE (1957) Concluding remarks. Cold Spring Harb Symp Quant Biol 22:415–427Google Scholar
  63. Jezkova T, Wiens JJ (2018) Testing the role of climate in speciation: new methods and applications to squamate reptiles (lizards and snakes). Mol Ecol 27:2754–2769Google Scholar
  64. Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066Google Scholar
  65. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Mentjies P, Drummond A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28(12):1647–1649. Google Scholar
  66. Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120Google Scholar
  67. Knapp S, Mallet J (2003) Refuting refugia? Science 300(5616):71–72Google Scholar
  68. Kozak KH, Graham CH, Wiens JJ (2008) Integrating GIS-based environmental data into evolutionary biology. Trends Ecol Evol 23(3):141–148Google Scholar
  69. Latrubesse EM, Cozzuol M, Silva-Caminha SAF, Rigsby CA, Absy MA, Jaramillo C (2010) The late Miocene paleogeography of the Amazon Basin and the evolution of the Amazon River system. Earth Sci Rev 99:99–124Google Scholar
  70. Leite RN, Rogers DS (2013) Revisiting Amazonian phylogeography: insights into diversification hypotheses and novel perspectives. Org Divers Evol 13:639–664. Google Scholar
  71. Leite RN, Kolokotronis SO, Almeida FC, Werneck FP, Rogers DS, Weksler M (2014) In the wake of invasion: tracing the historical biogeography of the South American cricetid radiation (Rodentia, Sigmodontinae). PLoS ONE 9(10):e110081. Google Scholar
  72. Leite YL, Costa LP, Loss AC, Rocha RG, Batalha-Filho H, Bastos AC, Quaresma VS, Fagundes V, Paresque R, Passamani M, Pardini R (2016) Neotropical forest expansion during the last glacial period challenges refuge hypothesis. Proc Natl Acad Sci 113(4):1008–1013Google Scholar
  73. Lima NE, Lima-Ribeiro MS, Tinoco CF, Terribile LC, Collevatti RG (2014) Phylogeography and ecological niche modelling, coupled with the fossil pollen record, unravel the demographic history of a Neotropical swamp palm through the Quaternary. J Biogeogr 41(4):673–686Google Scholar
  74. Martínez-Meyer E, Townsend Peterson A, Hargrove WW (2004) Ecological niches as stable distributional constraints on mammal species, with implications for Pleistocene extinctions and climate change projections for biodiversity. Glob Ecol Biogeogr 13(4):305–314Google Scholar
  75. Mayr E (1970) Populations, species and evolution: an abridgment of animal species and evolution. Harvard University Press, Cambridge. ISBN 0674690133Google Scholar
  76. Miranda GB, Miranda-Andrades J, Oliveira LFB, Langguth A, Mattevi MS (2007) Geographic patterns of genetic variation and conservation consequences in three South American rodents. Biochem Genet 45:839–856Google Scholar
  77. Moritz C (1994) Defining ‘evolutionarily significant units’ for conservation. Trends Ecol Evol 9:373–375Google Scholar
  78. Nabholz B, Glémin S, Galtier N (2007) Strong variations of mitochondrial mutation rate across mammals—the longevity hypothesis. Mol Biol Evol 25(1):120–130Google Scholar
  79. Nazareno AG, Dick CW, Lohmann LG (2017) Wide but not impermeable: testing the riverine barrier hypothesis for an Amazonian plant species. Mol Ecol 6:3636–3648Google Scholar
  80. Nitikman LZ, Mares MA (1987) Ecology of small mammals in a gallery forest of central Brazil. Ann Carnegie Mus 56(2):75–95Google Scholar
  81. Nunes MS (2011) Filogeografia comparativa e diversidade genética de espécies do gênero Hylaeamys (Rodentia: Sigmodontidae). Dissertation, PPG em Biodiversidade Biológica, Universidade Federal do Amazonas (UFAM). Accessed Nov 2016
  82. Ogden R, Thorpe RS (2002) Molecular evidence for ecological speciation in tropical habitats. Proc Natl Acad Sci 99(21):13612–13615Google Scholar
  83. Olson DM, Dinerstein E, Wikramanayake ED, Burgess ND, Powell GVN, Underwood EC, D’Amico JA, Itoua I, Strand HE, Morrison JC, Loucks CJ, Allnutt TF, Ricketts TH, Kura Y, Lamoreux JF, Wettengel WW, Hedao P, Kassem KR (2001) Terrestrial ecoregions of the world: a new map of life on Earth. Bioscience 51(11):933–938Google Scholar
  84. Parada A, D’Elía G, Palma RE (2015) The influence of ecological and geographical context in the radiation of Neotropical sigmodontine rodents. BMC Evol Biol 15(1):172Google Scholar
  85. Pasch B, Bolker BM, Phelps SM (2013) Interspecific dominance via vocal interactions mediates altitudinal zonation in Neotropical singing mice. Am Nat 182(5):E161–E173Google Scholar
  86. Patton JL, Da Silva MNF, Malcolm JR (1994) Gene genealogy and differentiation among arboreal spiny rats (Rodentia: Echimyidae) of the Amazon basin: a test of the riverine barrier hypothesis. Evolution 48(4):1314–1323Google Scholar
  87. Patton JL, Da Silva MNF, Malcolm JR (2000) Mammals of the Rio Juruá and the evolutionary and ecological diversification of Amazonia. Bull Am Mus Nat Hist 244:306Google Scholar
  88. Pearson RG (2010) Species’ distribution modeling for conservation educators and practitioners. Lessons Conserv 3:54–89Google Scholar
  89. Pearson RG, Raxworthy CJ, Nakamura M, Townsend Peterson A (2007) Predicting species distributions from small numbers of occurrence records: a test case using cryptic geckos in Madagascar. J Biogeogr 34(1):102–117Google Scholar
  90. Percequillo AR (2015) Genus Hylaeamys Weksler, Percequillo, and Voss, 2006. In: Gardner AL, Patton JL, Pardiñas UFJ, D’Elía G (eds) Mammals of South America, volume 2: Rodents. University of Chicago Press, Chicago. ISBN 978-0-226-16957-6Google Scholar
  91. Peres CA, Patton JL, da Silva MNF (1996) Riverine barriers and gene flow in Amazonian saddle-back tamarins. Folia Primatol 67:113–124. Google Scholar
  92. Peterson AT (2011) Ecological niche conservatism: a time-structured review of evidence. J Biogeogr 38:817–827Google Scholar
  93. Peterson AT, Nyári AS (2008) Ecological niche conservatism and Pleistocene refugia in the thrush-like mourner, Schiffornis sp., in the Neotropics. Evolution 62(1):173–183Google Scholar
  94. Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 190:31–259Google Scholar
  95. Pomara LY, Ruokolainen K, Young KR (2014) Avian species composition across the Amazon River: the roles of dispersal limitation and environmental heterogeneity. J Biogeogr 41(4):784–796Google Scholar
  96. Prado JR, Percequillo AR (2013) Geographic distribution of the genera of the tribe Oryzomyini (Rodentia: Cricetidae: Sigmodontinae) in South America: patterns of distribution and diversity. Arq Zool 44(1):1–120Google Scholar
  97. Pyron RA, Costa GC, Patten MA, Burbrink FT (2015) Phylogenetic niche conservatism and the evolutionary basis of ecological speciation. Biol Rev 90(4):1248–1262Google Scholar
  98. R Development Core Team (2008) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0Google Scholar
  99. Radosavljevic A, Anderson RP (2014) Making better Maxent models of species distributions: complexity, overfitting and evaluation. J Biogeogr 41(4):629–643Google Scholar
  100. Rambaut A (2012) FigTree v. 1.4.0. Accessed Nov 2016
  101. Rambaut A, Suchard MA, Xie D, Drummond AJ (2014) Tracer v1.6.
  102. Ribas CC, Aleixo A, Nogueira ACR, Miyaki CY, Cracraft J (2012) A palaeobiogeographic model for biotic diversification within Amazonia over the past three million years. Proc R Soc B 279:681–689Google Scholar
  103. Rissler LJ, Apodaca JJ (2007) Adding more ecology into species delimitation: ecological niche models and phylogeography help define cryptic species in the black salamander (Aneides flavipunctatus). Syst Biol 56(6):924–942Google Scholar
  104. Rocha RG, Ferreira E, Fonseca C, Justino J, Yuri LRL, Costa LP (2014) Seasonal flooding regime and ecological traits influence genetic structure of two small rodents. Ecol Evol 4(24):4598–4608Google Scholar
  105. Rossetti DF (2014) The role of tectonics in the late quaternary evolution of Brazil’s Amazonian landscape. Earth Sci Rev 139:362–389Google Scholar
  106. Rossetti DF, Valeriano MM (2007) Evolution of the lowest Amazon basin modeled from the integration of geological and SRTM topographic data. CATENA 70(2):253–265Google Scholar
  107. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  108. Savit AZ, Bates JM (2015) Right around the Amazon: the origin of the circum-Amazonian distribution in Tangara cayana. Folia Zool 64(3):273–283Google Scholar
  109. Schluter D (2000) The ecology of adaptive radiation. Oxford University Press, Oxford. ISBN 019850523XGoogle Scholar
  110. Schoener TW (1968) The Anolis lizards of Bimini: resource partitioning in a complex fauna. Ecology 49:704–726Google Scholar
  111. Seddon N, Tobias JA (2007) Song divergence at the edge of Amazonia: an empirical test of the peripatric speciation model. Biol J Linn Soc 90(1):173–188Google Scholar
  112. Shaw KL (2002) Conflict between nuclear and mitochondrial DNA phylogenies of a recent species radiation: what mtDNA reveals and conceals about modes of speciation in Hawaiian crickets. Proc Natl Acad Sci 99(25):16122–16127Google Scholar
  113. Silva CR, Ribas CC, Da Silva MNF, Leite RN, Catzeflis F, Rogers DS, De Thoisy B (2018) The role of Pleistocene climate change in the genetic variability, distribution and demography of Proechimys cuvieri and P. guyannensis (Rodentia: Echmyidae) in the northeastern Amazonia. PLoS ONE 13(12):e0206660Google Scholar
  114. Smith MF, Patton JL (1993) The diversification of South American murid rodents: evidence from mitochondrial DNA sequence data for the akodontine tribe. Biol J Linn Soc 50:149–177Google Scholar
  115. Smith MF, Patton JL (1999) Phylogenetic relationships and the radiation of sigmodontine rodents in South America: evidence from cytochrome b. J Mamm Evol 6(2):89–128Google Scholar
  116. Soley-Guardia M, Radosavljevic A, Rivera JL, Anderson RP (2014) The effect of spatially marginal localities in modelling species niches and distributions. J Biogeogr 41(7):1390–1401Google Scholar
  117. Soley-Guardia M, Gutiérrez EE, Thomas DM, Ochoa-G J, Aguilera M, Anderson RP (2016) Are we overestimating the niche? Removing marginal localities helps ecological niche models detect environmental barriers. Ecol Evol 6(5):1267–1279Google Scholar
  118. Solomon SE, Bacci M Jr, Martins J Jr, Vinha GG, Mueller UG (2008) Paleodistributions and comparative molecular phylogeography of leafcutter ants (Atta spp.) provide new insight into the origins of Amazonian diversity. PLoS ONE 3(7):e2738Google Scholar
  119. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729Google Scholar
  120. Templeton AR (1980) The theory of speciation via the founder principle. Genetics 94(4):1011–1038Google Scholar
  121. Tonini JFR, Costa LP, Carnaval AC (2013) Phylogeographic structure is strong in the Atlantic Forest; predictive power of correlative paleodistribution models, not always. J Zool Syst Evol Res 51(2):114–121Google Scholar
  122. Vilela JF, Mello B, Voloch CM, Schrago CG (2014) Sigmodontine rodents diversified in South America prior to the complete rise of the Panamanian Isthmus. J Zool Syst Evol Res 52(3):249–256Google Scholar
  123. Vital H, Stattegger K (2000) Lowermost Amazon River: evidence of late quaternary sea-level fluctuations in a complex hydrodynamic system. Quatern Int 72(1):53–60Google Scholar
  124. Vogler AP, Desalle ROB (1994) Diagnosing units of conservation management. Conserv Biol 8:354–363Google Scholar
  125. Wallace AR (1854) On the monkeys of the Amazon. Proc Zool Soc Lond 20:107–110. Google Scholar
  126. Waples RS (1991) Pacific salmon, Oncorynchus spp. & the definition of “species” under the endangered species act. Mar Fish Rev 53:11–22Google Scholar
  127. Warren DL, Glor RE, Turelli M (2008) Environmental niche equivalency versus conservatism: quantitative approaches to niche evolution. Evolution 62(11):2868–2883Google Scholar
  128. Warren DL, Glor RE, Turelli M (2010) ENMTools: a toolbox for comparative studies of environmental niche models. Ecography 33(3):607–611. Google Scholar
  129. Weksler M, Percequillo AR, Voss RS (2006) Ten new genera of oryzomyine rodents (Cricetidae: Sigmodontinae). Am Mus Novitates 69(2):1–30Google Scholar
  130. Werneck FP, Gamble T, Colli GR, Rodrigues MT, Sites JW Jr (2012a) Deep diversification and long-term persistence in the South American ‘dry diagonal’: integrating continent-wide phylogeography and distribution modeling of geckos. Evol Int J Org Evol 66(10):3014–3034Google Scholar
  131. Werneck FP, Nogueira C, Colli GR, Sites JW, Costa GC (2012b) Climatic stability in the Brazilian Cerrado: implications for biogeographical connections of South American savannas, species richness and conservation in a biodiversity hotspot. J Biogeogr 39(9):1695–1706Google Scholar
  132. Werneck FP, Leite RN, Geurgas SR, Rodrigues MT (2015) Biogeographic history and cryptic diversity of saxicolous Tropiduridae lizards endemic to the semiarid Caatinga. BMC Evol Biol 15(1):94Google Scholar
  133. Wiens JJ (2004) Speciation and ecology revisited: phylogenetic niche conservatism and the origin of species. Evolution 58(1):193–197Google Scholar
  134. Wiens JJ (2011) The causes of species richness patterns across space, time, and clades and the role of “ecological limits”. Q Rev Biol 86(2):75–96Google Scholar
  135. Yu Y, Harris AJ, He XJ (2010) S-DIVA (statistical dispersal-vicariance analysis): a tool for inferring biogeographic histories. Mol Phylogenet Evol 56:848–850Google Scholar
  136. Zhang DX, Hewitt GM (1996) Nuclear integrations: challenges for mitochondrial DNA markers. Trends Ecol Evol 11:247–251Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Arielli Fabrício Machado
    • 1
    • 6
    Email author
  • Mário Silva Nunes
    • 2
  • Cláudia Regina Silva
    • 4
    • 5
  • Marcelo Augusto dos SantosJr.
    • 1
  • Izeni Pires Farias
    • 2
  • Maria Nazareth Ferreira da Silva
    • 3
  • Marina Anciães
    • 3
  1. 1.Programa de Pós-Graduação em EcologiaInstituto Nacional de Pesquisas da Amazônia – INPAManausBrazil
  2. 2.Laboratório de Evolução e Genética Animal - LEGALUniversidade Federal do Amazonas – UFAMManausBrazil
  3. 3.Coordenação de Pesquisas em Biodiversidade/COBIO e Coleções ZoológicasInstituto Nacional de Pesquisas da Amazônia – INPAManausBrazil
  4. 4.Programa de Pós-Graduação em Genética, Conservação e Biologia EvolutivaInstituto Nacional de Pesquisas da Amazônia – INPAManausBrazil
  5. 5.Laboratório de MamíferosInstituto de Pesquisas Científicas e Tecnológicas do Estado do Amapá - IEPAMacapáBrazil
  6. 6.Phylogenetic and Functional Ecology Lab (LEFF)Porto AlegreBrazil

Personalised recommendations