Abstract
Haffer’s (Science 165: 131–137, 1969) Pleistocene refuge theory has provided motivation for 50 years of investigation into the connections between climate, biome dynamics, and neotropical speciation, although aspects of the original theory are not supported by subsequent studies. Recent advances in paleoclimatology suggest the need for reevaluating the role of Quaternary climate on evolutionary history in tropical South America. In addition to the many repeated large-amplitude climate changes associated with Pleistocene glacial-interglacial stages (~40 kyr and 100 kyr cyclicity), we highlight two aspects of Quaternary climate change in tropical South America: (1) an east-west precipitation dipole, induced by solar radiation changes associated with Earth’s precessional variations (~20 kyr cyclicity); and (2) periods of anomalously high precipitation that persisted for centuries-to-millennia (return frequencies ~1500 years) congruent with cold “Heinrich events” and cold Dansgaard-Oeschger “stadials” of the North Atlantic region. The spatial footprint of precipitation increase due to this North Atlantic forcing extended across almost all of tropical South America south of the equator. Combined, these three climate modes present a picture of climate change with different spatial and temporal patterns than envisioned in the original Pleistocene refuge theory.
Responding to these climate changes, biomes expanded and contracted and became respectively connected and disjunct. Biome change undoubtedly influenced biotic diversification, but the nature of diversification likely was more complex than envisioned by the original Pleistocene refuge theory. In the lowlands, intermittent forest expansion and contraction led to species dispersal and subsequent isolation, promoting lineage diversification. These pulses of climate-driven biotic interchange profoundly altered the composition of regional species pools and triggered new evolutionary radiations. In the special case of the tropical Andean forests adjacent to the Amazon lowlands, new phylogenetic data provide abundant evidence for rapid biotic diversification during the Pleistocene. During warm interglacials and interstadials, lowland taxa dispersed upslope. Isolation in these disjunct climate refugia led to extinction for some taxa and speciation for others.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Absy ML, Cleef A, Fornier M, Servant M, Siffedine A, Da Silva MF, Soubies F, Suguio K, Turcq B, Van der Hammen T (1991) Mise en evidence de quatre phases d’ouverture de la foret dense dans le sud-est de L’Amazonie au cours des 60,000 dernieres annees. Premiere comparaison avec d'autres regions tropicales. C R Acad Sci II 312:673–678
Adeney JM, Christensen NL, Vicentini A, Cohn-Haft M (2016) White-sand ecosystems in Amazonia. Biotropica 48:7–23
Antonelli A, Nylander JAA, Persson C, Sanmartin I (2009) Tracing the impact of the Andean uplift on Neotropical plant evolution. Proc Natl Acad Sci U S A 106:9749–9754. https://doi.org/10.1073/pnas.0811421106
Antonelli A, Zizka A, Carvalho FA, Scharn R, Bacon CD, Silvestro D, Condamine FL (2018) Amazonia is the primary source of Neotropical biodiversity. Proc Natl Acad Sci U S A 115:6034–6039. https://doi.org/10.1073/pnas.1713819115
Arz HW, Patzold J, Wefer G (1998) Correlated millennial-scale changes in surface hydrography and terrigenous sediment yield inferred from last-Glacial marine deposits off Northeastern Brazil. Quat Res 50:157–166
Asner GP, Anderson CB, Martin RE, Tupayachi R, Knapp DE, Sinca F (2015) Landscape biogeochemistry reflected in shifting distributions of chemical traits in the Amazon forest canopy. Nat Geosci 8:567–573
Baker PA, Fritz SC (2015) Nature and causes of Quaternary climate variation of tropical South America. Quat Sci Rev 124:31–47
Baker PA, Seltzer GO, Fritz SC, Dunbar RB, Grove M, Tapia P, Cross S, Rowe H, Broda J (2001a) The history of South American tropical climate for the past 25,000 years. Science 291:640–643
Baker PA, Rigsby CA, Seltzer GO, Fritz SC, Lowenstein T, Bacher N, Veliz Y (2001b) Tropical climate changes at millennial and orbital timescales revealed by deep drilling on the South American Altiplano. Nature 409:698–701
Baker PA, Fritz SC, Dick CW, Eckert AJ, Horton BK, Manzoni S, Ribas CC, Garzione CN, Battisti DS (2014) The emerging field of geogenomics: constraining geologic problems with genetic data. Earth Sci Rev 135:38–47
Batalha-Filho H, Fjelsa J, Fabre P-H, Yumi C (2013) Connections between the Atlantic and the Amazonian forest avifaunas represent distinct historical events. J Ornithol 154:41–50
Behling H, Arz HW, Patzold J, Wefer G (2000) Late Quaternary vegetational and climate dynamics in northeastern Brazil, inferences from marine core GeoB 3104-1. Quat Sci Rev 19:981–994
Berry PE, Riina R (2005) Insights into the diversity of the Pantepui Flora and the biogeographic complexity of the Guayana Shield. Biologiske Skrifter 5:145–167
Black DE, Peterson LT, Overpeck JT, Kaplan A, Evans MN, Kashgarian M (1999) Eight centuries of North Atlantic Ocean atmosphere variability. Science 286:1709–1713
Bouimetarhan I, Chiessi C, Gonzalez-Arango CG, Dupont L, Voigt I, Prange M, Zonneveld K (2018) Intermittent development of forest corridors in northeastern Brazil during the last deglaciation: climatic and ecologic evidence. Quat Sci Rev 192:86–96
Broecker WS (1994) Massive iceberg discharges as triggers for global climate change. Nature 372:421–424
Burbridge RE, Mayle FE, Killeen TJ (2004) Fifty-thousand year vegetation and climate history of Noel Kempff Mercado National Park, Bolivian Amazon. Quat Res 61:215–230
Bush MB (1994) Amazonian speciation: a necessarily complex model. J Biogeogr 21:5–18
Bush MB, De Oliveira PE, Colinvaux PA, Miller MC, Moreno JE (2004) Amazonian paleoecological histories: one hill, three watersheds. Palaeogeogr Palaeoclimatol Palaeoecol 214:359–393
Byrne H, Rylands AB, Carneiro JC, Alfaro JWL, Bertuol F, Silva MNF, Messias M, Groves CP, Mittermeier RA, Farias I, Hrbek T, Schneider H, Sampaio I, Boubli JP (2016) Phylogenetic relationships of the New World titi monkeys (Callicebus): first appraisal of taxonomy based on molecular evidence. Front Zool 13:10. https://doi.org/10.1186/s12983-016-0142-4
Capurucho JMG, Cornelius C, Borges SH, Cohn-Haft M, Aleixo A, Metzger JP, Ribas CC (2013) Combining phylogeography and landscape genetics of Xenopipo atronitens (Aves: Pipridae), a white sand campina specialist, to understand Pleistocene landscape evolution in Amazonia. Biol J Linn Soc 110:60–76
Carnaval AC, Hickerson MJ, Haddad CFB, Rodrigues MT, Moritz C (2009) Stability predicts genetic diversity in the Brazilian Atlantic forest hotspot. Science 323:785–789
Carnaval AC, Waltari E, Rodrigues MT, Rosauer D, VanDerWal J, Damasceno R, Prates I, Strangas M, Spanos Z, Rivera D, Pie MR, Firkowski CR, Bornschein MR, Ribero LF, Moritz C (2014) Prediction of phylogeographic endemism in an environmentally complex biome. Proc R Soc B 281:20141461
Cheng H, Sinha A, Cruz FW, Wang X, Edwards LR, d’Horta FM, Ribas CC, Vuille M, Stott LD, Auler AS (2013) Climate change patterns in Amazonia and biodiversity. Nat Commun 4:1411
Colinveaux PA, DeOlivera PE, Moreno JE, Miller MC, Bush MB (1996) A long pollen record from lowland Amazonia: forest cooling in Glacial times. Science 274:85–88
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
Cross S, Baker P, Seltzer G, Fritz S, Dunbar R (2001) Late Quaternary climate and hydrology of tropical South America inferred from an isotopic and chemical model of Lake Titicaca, Bolivia and Peru. Quat Res 56:1–9
Cruz FWJ, Burns SJ, Karmann I, Sharp WD, Vuille M, Cardoso AO, Ferrari JA, Silva Dias PL, Viana OJ (2005) Insolation-driven changes in atmospheric circulation over the past 116,000 years in subtropical Brazil. Nature 434:63–66
Cruz FW, Vuille M, Burns SJ, Wang X, Cheng H, Werner M, Edwards RL, Karmann I, Auler AS, Nguyen H (2009) Orbitally driven east-west anti-phasing of South American precipitation. Nat Geosci 2:210–214
D’Apolito CD, Absy ML, Latrubesse EM (2017) The movement of pre-adapted cool taxa in north-central Amazonia during the last glacial. Quat Sci Rev 169:1–12
Dal-Vechio F, Prates I, Grazziotin FG, Zaher H, Rodrigues MT (2018) Phylogeography and historical demography of the arboreal pit viper Bothrops bilineatus (Serpentes, Crotalinae) reveal multiple connections between Amazonian and Atlantic rainforests. J Biogeogr 45:2415–2426
Dansgaard W, Johnsen SJ, Clausen HB, Dahl-Jensen D, Gunderstrup NS, Hammer CU, Hvidberg CS, Steffensen JP, Sveinbjirnsdottir AE, Jouzel J, Bond G (1993) Evidence for general instability of past climate from a 250-year ice core record. Nature 364:218–220
Dexter KG, Lavin M, Torke BM, Twyford AD, Kursar TA, Coley PD, Drake C, Hollands R, Pennington RT (2017) Dispersal assembly of rain forest tree communities across the Amazon basin. Proc Natl Acad Sci U S A 114:2645–2650. https://doi.org/10.1073/pnas.1613655114
Dupont L, Schlutz F, Ewah CT, Jennerjahn TC, Pal A, Behling H (2010) Two-step vegetation response to enhanced precipitation in Northeast Brazil during Heinrich event 1. Glob Chang Biol 16:1647–1660
Erkens RHJ, Chatrou LW, Maas JW (2007) A rapid diversification of rainforest trees (Guatteria; Annonaceae) following dispersal from Central into South America. Mol Phylogenet Evol 44:399–411. https://doi.org/10.1016/j.ympev.2007.02.017
Esquivel-Muelbert A, Baker TR, Dexter KG (2019) Compositional response of Amazon forests to climate change. Glob Chang Biol 25:39–56
Fritz SC, Baker PA, Seltzer GO, Ballantyne A, Tapia P, Cheng H, Edwards L (2007) Quaternary glaciation and hydrologic variation in the South American tropics as reconstructed from the Lake Titicaca drilling project. Quat Res 68:410–420
Fritz SC, Baker PA, Ekdahl E, Seltzer GO, Stevens LR (2010) Millennial-scale climate variability during the Last Glacial period in the tropical Andes. Quat Sci Rev 29:1017–1024
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 41:1631–1638
Gentry A (1982) Neotropical floristic diversity: phytogeographical connections between Central and South America. Pleistocene climatic fluctuations or an accident of Andean orogeny? Ann Mo Bot Gard 69:557–593
Haffer J (1969) Speciation in Amazonian forest birds. Science 165:131–137
Hemming SR (2004) Heinrich events: massive late Pleistocene detritus layers of the North Atlantic and their global climate imprint. Rev Geophys 42(1):RG1005
Hermanowski B, Lima da Costa M, Carvalho AT, Behling H (2012) Palaeoenvironmental dynamics and underlying climatic changes in southeast Amazonia (Serra Sul dos Carajas, Brazil) during the late Pleistocene and Holocene. Palaeogeogr Palaeoclimatol Palaeoecol 365–366:227–246
Hoorn C, Wesselingh FP, ter Steege H, Bermudez MA, Mora A, Sevink J, Sanmartin I, Sanchez-Meseguer A, Anderson CL, Figueiredo JP, Jaramillo C, Riff D, Negri FR, Hooghiemstra H, Lundberg J, Stadler T, Sarkinen T, Antonelli A (2010) Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity. Science 330:927–931
Hughes C, Eastwood R (2006) Island radiation on a continental scale: exceptional rates of plant diversification after uplift of the Andes. Proc Natl Acad Sci 103:10334–10339
Jenkins CN, Pimm SL, Joppa LN (2013) Global patterns of terrestrial vertebrate diversity and conservation. Proc Natl Acad Sci 110(28):E2602–E2610
Kanner LC, Burns SJ, Cheng H, Edwards RL (2012) High-latitude forcing of the South American Summer Monsoon during the last Glacial. Science 335:570–573
Kay KM, Reeves PA, Olmstead RG, Schemske DW (2005) Rapid speciation and the evolution of hummingbird pollination in neotropical Costus subgenus Costus (Costaceae): evidence from nrDNA its and ETS sequences. Am J Bot 92:1899–1910. https://doi.org/10.3732/ajb.92.11.1899
Koenen EJM, Clarkson JJ, Pennington TD, Chatrou LW (2015) Recently evolved diversity and convergent radiations of rainforest mahoganies (Meliaceae) shed new light on the origins of rainforest hyperdiversity. New Phytol 207:327–339. https://doi.org/10.1111/nph.13490
Lagomarsino LP, Condamine FL, Antonelli A, Mulch A, Davis CC (2016) The abiotic and biotic drivers of rapid diversification in Andean bellflowers (Campanulaceae). New Phytol 210:1430–1442. https://doi.org/10.1111/nph.13920
Lavin M (2006) Floristic and geographical stability of discontinuous seasonally dry tropical forests explains patterns of plant phylogeny and endemism. In: Pennington RT, Lewis GP, Ratter JA (eds) Neotropical savannas and seasonally dry forests: plant diversity, biogeography and conservation. CRC Press, Boca Raton, FL, pp 433–448
Ledru MP, Ceccantini G, Gouveia S, Lopez-Saez JA, Pessenda L, Ribero AS (2006) Millennial-scale climatic and vegetation changes in a northern Cerrado (northeast Brazil) since the Last Glacial Maximum. Quat Sci Rev 25:1110–1126
Leite YLR, 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 last glacial period challenges refuge hypothesis. Proc Natl Acad Sci U S A 113:1008–1013
Liebsch D, Marques MC, Goldenberg R (2008) How long does the Atlantic Rain Forest take to recover after a disturbance? Changes in species composition and ecological features during secondary succession. Biol Conserv 141:1717–1725
Lisiecki LE, Raymo ME (2005) A Pliocene-Pleistocene stack of 57 globally distributed benthic δ18O records. Palaeoceanography 20:PA1003
Liu X, Battisti DS (2015) The influence of orbital forcing of tropical insolation on the climate and isotopic composition of precipitation in South America. J Clim 28:4841–4862
Luebert F, Wiegend W (2014) Phylogenetic insights into Andean plant diversification. Front Ecol Evol 2:article 27. https://doi.org/10.3389/fevo.2014.00027
Madriñán S, Cortés AJ, Richardson JE (2013) Páramo is the world’s fastest evolving and coolest biodiversity hotspot. Front Genet 4:192
McGee D, Moreno-Chamarro E, Green B, Marshall J, Galbraith E, Bradtmiller L (2018) Hemispherically asymmetric trade wind changes as signatures of past ITCZ shifts. Quat Sci Rev 180:214–228
Moritz C, Patton JL, Schneider CJ, Smith TB (2000) Diversification of rainforest faunas: an integrated molecular approach. Annu Rev Ecol Syst 31:533–563
Mosblech NAS, Bush MB, Gosling WD, Hodell DA, Thomas L, van Calsteren P, Correa-Metrio A, Valencia BG, Curtis J, van Woesik R (2012) North Atlantic forcing of Amazonian precipitation during the last ice age. Nat Geosci 5:817–820
Nace TE, Baker PA, Dwyer GS, Silva CG, Rigsby CA, Burns SJ, Giosan L, Ott-Bliesner B, Liu Z, Zhu J (2014) The role of North Brazil Current transport in the paleoclimate of the Brazilian Nordeste margin and paleoceanography of the western tropical Atlantic during the late Quaternary. Palaeogeogr Palaeoclimatol Palaeoecol 415:3–13
Pedro JB, Jochum M, Buizert C, He F, Barker S, Rasmussen SO (2018) Beyond the bipolar seesaw: toward a process understanding of interhemispheric coupling. Quat Sci Rev 192:27–46
Pennington RT, Prado DE, Pendry CA (2000) Neotropical seasonally dry forests and Quaternary vegetation changes. J Biogeogr 27:261–273
Peterson LC, Haug GH, Hughen KA, Rohl U (2000) Rapid changes in the hydrologic cycle of the tropical Atlantic during the Last Glacial. Science 290:1947–1951
Phillips BL, Brown GP, Greenlees M, Webb JK, Shine R (2007) Rapid expansion of the cane toad (Bufo marinus) invasion front in tropical Australia. Austral Ecol 32:169–176
Pouchon C, Fernández A, Nassar JM, Boyer F, Aubert S, Lavergne S, Mavárez J (2018) Phylogenomic analysis of the explosive adaptive radiation of the Espeletia complex (Asteraceae) in the Tropical Andes. Syst Biol 67:1041–1060
Prado LF, Wainer I, Chiessi CM (2013) Mid-Holocene PMIP3/CMIP5 model results: intercomparison for the South American monsoon system. The Holocene 23:1915–1920
Prates I, Rodrigues MT, Melo-Sampaio PR, Carnaval AC (2015) Phylogenetic relationships of Amazonian anole lizards (Dactyloa): taxonomic implications, new insights about phenotypic evolution and the timing of diversification. Mol Phylogenet Evol 82:258–268
Prates I, Xue AT, Brown JL, Alvarado-Serrano DF, Rodrigues MT, Hickerson MJ, Carnaval AC (2016a) Inferring responses to climate dynamics from historical demography in neotropical forest lizards. Proc Natl Acad Sci 113:7978–7985
Prates I, Rivera D, Rodrigues MT, Carnaval AC (2016b) A mid-Pleistocene rainforest corridor enabled synchronous invasions of the Atlantic Forest by Amazonian anole lizards. Mol Ecol 25:5174–5186
Prates I, Penna A, Rodrigues MT, Carnaval AC (2018) Local adaptation in mainland anole lizards: integrating population history and genome-environment associations. Ecol Evol 8:11932–11944
Punyasena SW, Mayle FE, McElwain JC (2008) Quantitative estimates of glacial and Holocene temperature and precipitation change in lowland Amazonian Bolivia. Geology 36:667–670
Quijada-Mascareñas A, Ferguson JE, Pook CE, Wuster W (2007) Phylogeographic patterns of Trans-Amazonian vicariants and Amazonian biogeography: the Neotropical rattlesnake (Crotalus durissus complex) as an example. J Biogeogr 34:1296–1312
Rahmstorf S (2002) Ocean circulation and climate during the past 120,000 years. Nature 419:207
Rangel TF, Edwards NR, Holden PB, Diniz-Filho JAF, Gosling WD, Coelho MTP, Cassemiro FAS, Rahbek C, Colwell RK (2018) Modeling the ecology and evolution of biodiversity: biogeographic cradles, museums, and graves. Science 361:244
Reis LS, Guimaraes J, Souza-Filho P, Sahoo PK, Figueiredo M, Giannini T (2017) Environmental and vegetation changes in southeastern Amazonia during the late Pleistocene and Holocene. Quat Int 449:83–105
Richardson JE, Pennington RT, Pennington TD, Hollingsworth PM (2001) Rapid diversification of a species-rich genus of neotropical rain forest trees. Science 293:2242–2245
Rull V, Carnaval AC (2019) Introduction. In: Rull V, Carnaval A (eds) Neotropical diversification. Springer, Heidelberg
Santos JC, Coloma LA, Summers K, Caldwell JP, Ree R, Cannatella DC (2009) Amazonian amphibian diversity is primarily derived from late Miocene Andean lineages. PLoS Biol 7(3):e1000056
Schrag DP, Adkins JF, McIntyre K, Alexander JL, Hodell DA, Charles CD, McManus JF (2002) The oxygen isotopic composition of seawater during the Last Glacial Maximum. Quat Sci Rev 21:331–342
Steig E, Alley R (2002) Phase relationships between Antarctic and Greenland climate records. Ann Glaciol 35:451–456
Stodart E, Parer I (1988) Colonisation of Australia by the rabbit Oryctolagus cuniculus (L.). CSIRO, Canberra
Stute M, Forster M, Frischkorn H, Serejo CP, Broecker WS (1995) Cooling of tropical Brazil during the last glacial maximum. Science 269:379–383
Sylvestre F, Servant M, Servant-Vildary S, Causse C, Fournier M, Ybert JP (1999) Lake-level chronology on the southern Bolivian Altiplano (18–23°S) during late-Glacial time and the early Holocene. Quat Res 51:54–66
van der Hammen T, Cleef AM (1986) Development of the high Andean páramo flora and vegetation. In: Vuilleumier F, Monasterio M (eds) High altitude tropical biogeography. Oxford University Press, New York, pp 153–201
Vanzolini P, Williams E (1970) South American anoles: the geographic differentiation and evolution of the anolis Chrysolepis species group (Sauria, Iguanidae). Arquivos de Zoologia 19:125–298
Vargas OM, Dick CW (2019) Diversification history of Neotropical Lecythidaceae, an ecologically dominant tree family of Amazon rain forest. In: Rull V, Carnaval A (eds) Neotropical diversification. Springer, Heidelberg
Vargas OM, Simpson BB (2019) Allopatric speciation versus parapatric ecological divergence in high Andean plants (Asteraceae: Piofontia). bioRxiv:868216. https://doi.org/10.1101/868216
Vellinga M, Wood RA (2002) Global climatic impacts of a collapse of the Atlantic thermohaline circulation. Clim Chang 54:251–267
Voelker AH (2002) Global distribution of centennial-scale records for Marine Isotope Stage (MIS) 3: a database. Quat Sci Rev 21:1185–1212
Wang X, Edwards RL, Auler AS, Cheng H, Kong X, Wang Y, Cruz FW, Dorale JA, Chiang H-W (2017) Hydroclimate changes across the Amazon lowlands over the past 45,000 years. Nature 541:204–207
Wehtje W (2003) The range expansion of the great-tailed grackle (Quiscalus mexicanus Gmelin) in North America since 1880. J Biogeogr 30:1593–1607
Wheatley A et al (2019) Modeling the origins of biodiversity in the tropical Andes (manuscript in preparation)
Wiens JJ (2004) Speciation and ecology revisited: phylogenetic niche conservatism and the origin of species. Evolution 58:193–197
Zhang Y, Chiessi CM, Mulitza S, Sawakuchi AO, Haggi C, Zabel M, Portioho-Ramos C, Schefuß E, Crivellari S, Wefer G (2017) Different precipitation patterns across tropical South America during Heinrich and Dansgaard-Oeschger stadials. Quat Sci Rev 177:1–9
Acknowledgements
Writing of the manuscript was supported by a NASA workshop grant (NASA 15-BIODIV15-0013) to SF, as well as by NSF EAR-1338694 to PB, SF, DB, and CD. We are grateful to the Charles Darwin Foundation, Galapagos for their support during the writing of an initial version of this manuscript. John Megahan, University of Michigan, assisted with graphics.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2020 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Baker, P.A. et al. (2020). Beyond Refugia: New Insights on Quaternary Climate Variation and the Evolution of Biotic Diversity in Tropical South America. In: Rull, V., Carnaval, A. (eds) Neotropical Diversification: Patterns and Processes. Fascinating Life Sciences. Springer, Cham. https://doi.org/10.1007/978-3-030-31167-4_3
Download citation
DOI: https://doi.org/10.1007/978-3-030-31167-4_3
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-31166-7
Online ISBN: 978-3-030-31167-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)