Molecular Ecology (2012)                                                                                  doi: 10.1111/mec...
2 A. C. TURCHETTO-ZOLET ET AL.transgressions, have impacted this continent, creating          result, an increasing number...
PHYLOGEOGRAPHY OF SOUTH AMERICA 3Carvalho  Almeida 2010; Nullo  Combina 2011; Ru-                                         ...
4 A. C. TURCHETTO-ZOLET ET AL.contraction), (v) hypothesized refugia types (multiple or           region (temperate vs. tr...
PHYLOGEOGRAPHY OF SOUTH AMERICA 5as Chagas disease (Reduviidae) and malaria (Culicidae).         (see Fig. 2). For instanc...
6 A. C. TURCHETTO-ZOLET ET AL.                                                   0.005%                             (a)   ...
PHYLOGEOGRAPHY OF SOUTH AMERICA 7(Fittkau et al. 1969); and two subregions (Kuschel 1969),                                ...
8 A. C. TURCHETTO-ZOLET ET AL.                                                                                        Fig....
PHYLOGEOGRAPHY OF SOUTH AMERICA 9much discussion (Bush  de Oliveira 2006). What               not necessarily correspond t...
10 A . C . T U R C H E T T O - Z O L E T E T A L .(fish: Zemlak et al. 2008; birds: Gonzalez  Wink 2010;           distribu...
P H Y L O G E O G R A P H Y O F S O U T H A M E R I C A 11et al. 2011) have been reported to be effective barriers        ...
12 A . C . T U R C H E T T O - Z O L E T E T A L .is the cryptic speciation within a well-connected system         the maj...
P H Y L O G E O G R A P H Y O F S O U T H A M E R I C A 13gested as dispersal corridors (Zemlak et al. 2008). A         o/...
Filogeografia en Suramerica
Filogeografia en Suramerica
Filogeografia en Suramerica
Filogeografia en Suramerica
Filogeografia en Suramerica
Filogeografia en Suramerica
Filogeografia en Suramerica
Filogeografia en Suramerica
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Filogeografia en Suramerica

  1. 1. Molecular Ecology (2012) doi: 10.1111/mec.12164INVITED REVIEW AND META-ANALYSESPhylogeographical patterns shed light on evolutionaryprocess in South AmericaA . C . T U R C H E T T O - Z O L E T , * F . P I N H E I R O , † F . S A L G U E I R O ‡ and C . P A L M A - S I L V A †*Programa de Ps-Graduac~o em Gentica e Biologia Molecular, Departamento de Gentica, IB/UFRGS, 91501-970, Porto o ßa e eAlegre, RS, Brazil, †Instituto de Bot^nica, Av. Miguel Stefano 3687, Agua Funda, 04301-902, S~o Paulo, SP, Brazil, a a‡Departamento de Bot^nica, UNIRIO, 22290-240, Rio de Janeiro, RJ, Brazil a Abstract The South American continent is composed of several biogeographical regions harbouring the highest biodiversity on the globe, encompassing five of the world’s biodiversity ‘hot spots’. Nonetheless, the patterns and processes responsible for shap- ing its astonishing species diversity are largely unknown. Here, we present a review of current South American phylogeographical knowledge based on published articles on this topic. An appraisal of the literature reveals emerging phylogeographical patterns in the biota of South America. The striking phylogeographical divergence observed among organism lineages in South American studies is suggestive of high levels of undocumented species diversity. The interplay between Pleistocene climatic oscilla- tions and Pliocene/Miocene orogenic events has contributed to shaping the current diversity and distribution of modern lineages in both the tropical and temperate regions of South America. Although older divergence times were observed for a range of species, most herpetofauna underwent an intraspecific lineage split much earlier than other organisms. The geographical ranges of species associated with forest habi- tats were reduced mainly during glacial cycles, whereas species associated with open vegetation domains have shown variable responses to climatic oscillations. The results suggest a highly complex mosaic of phylogeographical patterns in South America. We suggest future research directions to promote a better understanding of the origin and maintenance of the South American biota. Keywords: biodiversity, microevolution, neotropics, phylogeography, population structure, species diversification Received 28 January 2012; revision received 31 October 2012; accepted 6 November 2012 chains (i.e. the Andean Cordillera) (Clapperton 1993).Introduction South America harbours the greatest biodiversity onSouth America is a large continent extending over a Earth, containing five of the world’s biodiversity ‘hotwide latitudinal range (between 12°N and 56°S) that spots’ (Myers et al. 2000). Furthermore, South Americaincludes an extensive variety of climates, closely associ- is a biogeographically diverse continent composed of aated with vegetation formation. The more extensive variety of different biomes/ecoregions (Morrone 2004,northern part, located near the equatorial zone, is tropi- 2006; Aragon et al. 2011). The diversification processescal, whereas the narrower southern part has subtropical on this continent cannot be restricted to a particularand cool temperate climates (Fittkau et al. 1969; Sylves- time interval or mechanism (Rull 2011). The evolution-tre 2009; Aragon et al. 2011). The continent also shows ary history of South America has been linked to a suc-complex geomorphological patterns, such as large river cession of major geological events that have modifiedplains (i.e. the Amazon basin) and extensive mountain both continents and oceans (Graham 2009; Cavallotto et al. 2011; Folguera et al. 2011; Lavina Fauth 2011).Correspondence: Clarisse Palma-Silva, Fax: +551150733678; Climate changes and associated glaciations, as well asE-mail: palaeobasins and shifting shorelines due to marine© 2012 Blackwell Publishing Ltd
  2. 2. 2 A. C. TURCHETTO-ZOLET ET AL.transgressions, have impacted this continent, creating result, an increasing number of studies have been pub-complex scenarios for species diversification (Colinvaux lished. Nevertheless, comparative phylogeographicalet al. 1996; Behling 2002; Antonelli Sanmartin 2011; studies are still needed. Recent reviews of the phylogeo-Aragon et al. 2011; Compagnucci 2011). graphical patterns within some specific areas in South Much effort has been put into understanding the America have been published (e.g. Brazilian Atlanticcomplex and high levels of biodiversity in South Amer- Rainforest: Martins 2011; Silva et al. 2012; Amazon:ica. Phylogeographical studies of South American taxa Antonelli et al. 2010; Aleixo Rossetti 2007; Pampasmay provide valuable insight into the historical grassland: Fregonezi et al. 2012; Patagonia: Srsic et al. eprocesses underlying diversification in this region. 2011; Pardi~ as et al. 2011; Albino 2011). However, no nMolecular analyses based on DNA sequence variations attempt has been made to compare these patternsin living organisms together with advances in statistical across the major regions of the continent.phylogeography have shed further light on how geolog-ical events and climatic changes have modified the Geological history and climatic changes indemographic history of populations (Avise 2009). Such South Americaphylogeographical studies can provide a better under-standing of the biodiversity, dispersal modes, diversifi- The structural framework of the continent was formedcation times, extinctions, refugia areas and other by the distribution and interplay of several majorspecies-/population-level processes (microevolutionary geotectonic units, which include the following classes:processes; reviewed by Diniz-Filho et al. 2008). In addi- cratons (Guiana, Central Brazilian and Coastal Braziliantion, comparative phylogeography may provide infor- shields), intercratonic basins (Amazonas, Parnaiba, Saomation regarding significant historical events that have Francisco and Parana), pericratonic basins (Llanos-a common influence on many species and may indicate Iquitos-Acre-Beni-Chaco-Pampas plains), nesocratonscommon biotic responses to historical climatic and (Pampean Ranges, Patagonia and Deseado massifs) andgeomorphological processes (Bermingham Moritz geosynclines (Andean belts) (Harrington 1962).1998). These studies are able to detect the regional- and The geological isolation and long-term climatic stabil-landscape-level biodiversity patterns that are important ity that have affected the South American continentfor understanding macroecology, the broad impacts of would have favoured the gradual accumulation of biodi-geological events and areas of high conservation prior- versity over time (Mittelbach et al. 2007). Long periodsity (Bermingham Moritz 1998; Moritz 2002). Thus, of time marked the separation of the continents, whichphylogeography provides insights into the processes were associated with episodes of volcanism, uplift andinvolved in the origin and distribution of biodiversity. subsidence of large areas. These are important elementsExamples of the contributions of phylogeographical of the geological history of South America and continuestudies to the understanding of evolutionary processes to occur (Clapperton 1993). The Andean uplift began inon large scales were recently reviewed for Europe (Tab- the late Oligocene to early Miocene (about 23 Ma), buterlet et al. 1998; Nieto Feliner 2011), North America the most intense peak of Andean mountain building(Avise 2000; Soltis et al. 2006; Shafer et al. 2010), New occurred during the late middle Miocene (about 12 Ma)Zealand (Wallis Trewick 2009), southern Australia and early Pliocene (about 4.5 Ma) (Hoorn et al. 2010;(Byrne 2008) and Africa (Lorenzen et al. 2012). For Folguera et al. 2011). This mountain range extends forinstance, in the northern hemisphere, a large number of almost 9000 km along the western coast of South Amer-phylogeographical studies facilitated identification of ica. Elevation, particularly in the Andes, is an importantmajor Pleistocene refugia, cryptic refugia, demographic factor for climatic and ecological control in South Amer-expansion and many other species-/population-level ica (Hoorn et al. 1995). Thus, the Andean uplift greatlyaspects (Avise 2000; Cook et al. 2001; Lessa et al. 2003; influenced biodiversity organization in South AmericaSoltis et al. 2006; Shafer et al. 2010). This includes suture (Gentry 1982; Hoorn et al. 1995, 2010; Jørgensen Len- ozones–areas containing multiple hybrid and contact Ynez 1999; Antonelli et al. 2010). In their northern and azones (Remington 1968; Swenson Howard 2004). The central reaches, the Andes are quite wide and containnumber of phylogeographical studies of South America extensive plateaus, such as the Altiplano, and a numberis comparatively lower, despite it having one of the of major valleys (Folguera et al. 2011). The southernhighest levels of biodiversity on Earth (Beheregaray Andes have been eroded by the Patagonian ice sheet2008; Srsic et al. 2011). Until 2006, only 6.3% of all e and are much lower and narrower (Garzione et al. 2008;phylogeographical studies published worldwide were Hoorn et al. 2010; Lavina Fauth 2011). The complexdedicated to organisms from the South American conti- and dynamic geological history of South America is ofnent (Beheregaray 2008). The field of phylogeography great importance for understanding the origins of thehas recently blossomed in South America, and as a present-day high biodiversity (Clapperton 1993; De © 2012 Blackwell Publishing Ltd
  3. 3. PHYLOGEOGRAPHY OF SOUTH AMERICA 3Carvalho Almeida 2010; Nullo Combina 2011; Ru- Materials and methodszzante Rabassa 2011). Glacial and interglacial periods associated with past Literature surveyclimate changes may also have influenced the dynam-ics of biodiversity, dramatically altering the landscape The database used for this review was compiled byand evolution of South America. Glaciations have conducting searches in the Web of Science® (Institute ofoccurred at different time intervals and are influenced Scientific Information, Thomson Scientific). We firstby cyclic variations in the Earth’s orbit, known as Mil- searched articles published from 1987 (date regarded asankovitch cycles (Bartlein Prentice 1989; Berger the birth of phylogeography as discipline: Avise et al.Loutre 1989; Zachos et al. 2001). The orbital rhythms 1987) to 2011 using two key phrases: ‘phylogeograph*’act in combination, producing periodic variations in and ‘South America’. Because many studies did notthe distribution and intensity of sunlight. An alternat- mention ‘South America’, we also searched by eaching sequence of glacial and interglacial conditions has South American country individually. We have limitedcharacterized the second half of the Quaternary. Palae- our discussion to organisms that occur mainly in theovegetational reconstructions have recovered drastic South American continent. Thus, we did not considerpast vegetational changes due to glacial–interglacial studies in which the range of organisms was largelycycles (e.g. Colinvaux et al. 1996; Rull 1999; Behling outside of South America (e.g. Central and North2002; Iglesias et al. 2011; Quattrocchio et al. 2011). It America, New Zealand, Australia and Antarctica).has been argued that Quaternary glaciations may have Marine organism was not included when their rangesresulted in the fragmentation of forest land into extended beyond the South American coast. Studiesislands in a sea of savannas and/or deserts (refugia), that covered only a small part of a species geographicalpromoting lineage differentiation (Hooghiemstra van range were also excluded. Studies of invasive speciesder Hammen 1998), which may have promoted specia- and Amerindian populations were not considered.tion and diversification. For example, the refuge theory Articles with a purely taxonomic or systematic empha-of Amazonian speciation was based on the idea that sis were also excluded. Additionally, we excluded stud-climatic oscillations occurring during the Pleistocene ies in which the terms ‘phylogeography’,promoted allopatric/parapatric speciation (Haffer 1969, ‘phylogeographical’ or ‘phylogeographic’ appeared only2008; Prance 1973) and might have contributed to the in the keywords or title.high biodiversity in this area. However, this idea hasbecome controversial (Colinvaux et al. 2000; Bush de Review of South American phylogeographical patternsOliveira 2006) because it has been recognized thatTertiary Neogene tectonic and palaeogeographical reor- For all of the retrieved articles (Table 1), we recordedganization have also been important drivers of the ori- the following information: (i) sample taxa, (ii) moleculargin of Neotropical (Pennington et al. 2004; Hoorn et al. markers, (iii) main biome/ecoregion, (iv) inferred2010; Rull 2011) and temperate biodiversity (Quiroga demographic processes (population expansion or Premoli 2010; Srsic et al. 2011) in South America. e Here, we review current phylogeographical knowl- Table 1 Summary of the reviewed studies, including the totaledge of South America based on a detailed examina- number of papers, total number of species encounters andtion of published articles, discussing the main results number of studies per taxonomic categoriesin the light of the current debate concerning the prob-able agents responsible for the high level of biodiver- Category No of itemssity and its geographical distribution across the Total of studies 214different biogeographical regions in this continent (Ho- Total of taxa 476orn et al. 2010; Antonelli Sanmartin 2011; Rull 2011; Total of studies per taxonomic categorySrsic et al. 2011). Specifically, we had the following e Algae 2goals: (i) to review the current knowledge of phyloge- Plant 36ography in South America; (ii) to verify the occurrence Invertebrate* 29of demographic processes (expansion and contraction) Fish* 28related to glacial/interglacial climatic oscillations; (iii) Amphibian 20 Reptile 20to assess hypothesized refugia types (multiple or Bird 19single); and (iv) to discuss the role of geological and Mammal 61climatic changes during the Tertiary and Quaternaryin shaping the phylogeographical patterns of South *Note there is one study included in two taxonomic categories,America. see Table S2 (Supporting information) for details.© 2012 Blackwell Publishing Ltd
  4. 4. 4 A. C. TURCHETTO-ZOLET ET AL.contraction), (v) hypothesized refugia types (multiple or region (temperate vs. tropical/subtropical) and lineagesingle) and (vi) divergence times of the main phylo- splitting times by analysis of variance (ANOVA) using thegroups. Categorizing studies by biomes or ecoregions software SPSS 11.0 (SPSS, Inc., Chicago, IL, USA).was difficult because many authors have used political Second, we added organisms (taxonomic groups) asdivisions (i.e. countries, states, provinces) instead of predictor variables of lineage splitting times to refineecological divisions such as biomes, ecosystems or the analysis and identify additional patterns, also usingecoregions. Because our goal was not to provide a criti- ANOVA. Third, we used the chi-square test to assess thecal biogeographical review of South America, which strength of the association of glacial/interglacial periodshad previously been done by De Carvalho Almeida with forest-dwelling and open-habitat organisms. We(2010), we used the regionalizations used in each article. tested the association of population expansion vs. frag-The approximate distribution of major terrestrial South mentation during glacial and interglacial periods forAmerican biomes/ecoregions adopted in this review is forest-dwelling and open-habitat organisms.shown in Fig. 1 (modified from Olson et al. 2001; shape-file available at ( Results and discussiondata/item1875.html). Morrone (2010b) provided a com-prehensive review of South American regionalizations Literature surveyand their characteristics. Given that region, habitat type or latitude may relate The Web of Science® survey of the literature from 1987to important palaeoclimatic drivers of diversification, to 2011 identified 323 articles (excluding four reviews)we first tested for the relationship between climatic that focused on South American phylogeography. In addition, 678 studies were retrieved using country/ter- ritory names. When used as a keyword, Brazil was the most listed country with 219 articles, followed by Argentina with 111, Chile with 79, Peru with 58, Vene- zuela with 46 and Ecuador with 40; other countries were listed no more than 30 times (Table S1, Supporting information). After excluding duplicates, 640 articles were identified. Focusing on species with a distribution range primarily encompassing South America and after the exclusion of articles that did not meet the require- ments described in the Materials and Methods section, 214 relevant studies were retrieved by our literature survey (Table S2, Supporting information). Overall, 476 taxa were studied (Table 1). Plants and vertebrates accounted for 86% of the phylogeographical studies, with other taxonomic groups comprising the remainder, including invertebrates (13%) and algae (1%). Among plants (a total of 36 articles), angiosperms constituted the majority (34 articles), compared with only two stud- Amazon ies of gymnosperms. Fabaceae (17%), Nothofagaceae Andes (12%), Asteraceae (9%), Araucariaceae (6%), Bromelia- Atlantic Forest Cerrado ceae (6%), Clusiaceae (6%), Meliaceae (6%), Proteaceae Patagonia/Monte Desert (6%) and Solanaceae (6%) were the most represented Chaco/Pantanal Orinoco plant families. Plant-rich families such as Lauraceae, Pampas Myrtaceae and Melastomataceae were not considered in Caatinga these phylogeographical studies. This bias may be Chocó Guiana Highlands related to the lack of specific molecular markers for use 400 km in population-level studies (Peakall 2007), mainly for plant families that do not have applied scientific or commercial uses.Fig. 1 Approximate distribution of major terrestrial South Most studies of invertebrates (a total of 29 articles)American biomes/ecoregions (modified from Olson et al. 2001)used in this study. See Morrone (2010b) for detailed revision focused on insects (65%), primarily the Culicidae (25%),regarding differences in the resolution and delimitations of Reduviidae (25%) and Formicidae (15%). Moreover,such biomes/ecoregions available in the literature. these concentrated on vectors of human diseases, such © 2012 Blackwell Publishing Ltd
  5. 5. PHYLOGEOGRAPHY OF SOUTH AMERICA 5as Chagas disease (Reduviidae) and malaria (Culicidae). (see Fig. 2). For instance, 67% of the studies recoveredCrustaceans and molluscs were represented by only in our review were conducted from 2007 to 2011.four studies each. Among vertebrates, mammals were One possible reason for the disparity in the numberthe largest taxonomic group studied, addressed in 61 of studies of plants (17%) and animals (82%) is thearticles (28%). Of those, 37% were focused on rodents, well-documented lack of polymorphisms in molecularand most were performed on multiple species using a markers available for intraspecific-level studies forcomparative approach (Da Silva Patton 1998; Costa plants compared with animals (Schaal Olsen 2000;2003; Lessa et al. 2010). Among rodents, Cricetidae were Brunsfeld et al. 2001; Soltis et al. 2006; among others).analysed in 54% of the studies, followed by Echimyidae Therefore, Sanger sequencing of mitochondrial DNA(23%). The other well-represented mammal groups (mtDNA) has predominated in phylogeographical stud-included Phyllostomidae (10%), Didelphidae (9%) and ies in South America (Fig. 3a). Approximately, 78% ofFelidae (7%). Fish were addressed in 13% of the studies all studies used mtDNA to infer phylogeogra-(a total of 28 articles). Galaxiidae species were exam- phical patterns: 58% of these used only the mtDNAined in 14% of the studies, Characidae (10%), Cichlidae genome, 15% combined mtDNA and nuDNA (including(7%), Percichthyidae (7%), Sciaenidae (7%) and Trich- sequencing of low-copy nuclear genes, AFLPs or ISSRs)omycteridae (7%). Lizards, snakes, turtles and crocodil- and 5% combined mtDNA and microsatellite loci. San-ians (reptiles) were investigated in 9% of the studies (20 ger sequencing of plastidial genome (cpDNA) regionsarticles), which focused primarily on the Liolaemidae was used in 13% of studies, most of which (59%) used(30%) and Viperidae (25%). Twenty studies were of only cpDNA. Four studies combined cpDNA and mi-amphibians (9%), primarily the Hylidae (36%), Bufoni- crosatellites, and another eighth applied a combinationdae (23%), Leptodactylidae (14%), Cycloramphidae (9%) of cpDNA and nuDNA. Lastly, a small proportion ofand Dendrobatidae (9%). Amphibians were also investi- articles (3%) referenced other marker combinations. Onegated extensively in comparative phylogeographical study used all three genomes (algae: Tellier et al. 2009);studies, providing strong support for the recovered data another used mtDNA, nuDNA and microsatellite loci(Carnaval 2002; Carnaval Bates 2007; Carnaval et al. (Culver et al. 2000); four applied mtDNA with karyo-2009; Thom et al. 2010). Birds were studied in 9% (total e types (Confalonieri et al. 1998; Pellegrino et al. 2005;of 19 articles) of the phylogeographical articles; these Garcia 2006; Bonvicino et al. 2009) or morphologicalconcentrated on Dendrocolaptidae (26%), Furnariidae measures (Puorto et al. 2001; Chaves et al. 2007) to(21%) and Psittacidae (15%). determine species-level phylogeographical patterns. These patterns were generally similar to those in Overall, 72% of the studies used only one type of molec-reports from other parts of the globe (Europe: Taberlet ular al. 1998; North America: Soltis et al. 2006; Shafer et al. Although it is now common practice for phylogeogra-2010; New Zealand: Wallis Trewick 2009; southern phy studies to use a diverse suite of markers (Toews Australia: Byrne 2008). Some differences between the Brelsford 2012), studies from South America did not fol-composition of our literature survey and the review of low this trend (Fig. 4). While the number of studies hasBeheregaray (2008), which included the entire southern increased over the years, the proportion that appliedhemisphere, might be attributable to the great increase only one molecular marker to those that applied bothin phylogeographical studies in South America since uniparental (organellar) and biparental (nuclear) inher-2006, the latest date included in Beheregaray’s report ited markers has not changed accordingly. This is 40 Fig. 2 Number of phylogeographical arti- cles published between 1987 and 2011 in 35 which organism distribution ranges 30 encompass primarily the South AmericanNumber of studies 25 continent. 20 15 10 5 0 Year© 2012 Blackwell Publishing Ltd
  6. 6. 6 A. C. TURCHETTO-ZOLET ET AL. 0.005% (a) (b) 1% 2% 5% 11% mtDNA 4% 58% cpDNA 27% nuDNA, RFLP, AFLP or 6% ISSR 15% Microssatelites Allozyme Tropical mtDNA and nuDNA Temperate (RFLP, AFLP or ISSR) Subtropical 0.005% cpDNA and nuDNA 1% More than one (RFLP, AFLP or ISSR) 4% climatic region mtDNA and SSR cpDNA and SSR 8% mtDNA, cpDNA and nuDNA 56% Other combinationsFig. 3 Percentage of phylogeography articles published between 1987 and 2011 according to (a) classes of genetic marker or markercombinations used (categories are mutually exclusive) and (b) type of environment (see text for details). 30 seed dispersal rates (Caetano et al. 2008; Palma-Silva One genome et al. 2009; Tremetsberger et al. 2009; Pinheiro et al. 25 Multiple genomesNumber of studies 2011); differences in the evolution rates and coalescence 20 times of nuclear and cytoplasmic markers (Cabanne 15 et al. 2008; Tellier et al. 2009); and introgressive hybrid- 10 ization of organellar markers (Dick Heuertz 2008; Acosta Premoli 2010; Palma-Silva et al. 2011). 5 The importance of evaluating multiple markers from 0 different genomes in any phylogeographical study is Year progressively becoming more evident. This idea is particularly applicable in South America, due to itsFig. 4 Phylogeographical studies between 1987 and 2011 show- poorly understood and complex historical phylogeo-ing the proportion per year of those that used a single genome graphy. The shift from single to multiple genome(black line) vs. multiple genomes (grey line). phylogeographical studies will greatly benefit from whole-genome sequencing technologies. As genomicimportant because the use of only one type of marker approaches become cheaper and sequencing technolo-to infer phylogeographical or phylogenetic relationships gies allow more efficient analysis, surveying differentmay not be sufficient to fully investigate certain taxa genomes and markers for population samples of non-(Avise Wollenberg 1997), risking generation of a gene model species will soon become feasible (Ekblom tree that does not represent the true relationships Galindo 2010).among taxa (Edwards Bensch 2009; Toews Brels- The variety of biomes and ecosystems across theford 2012). continent is a reflection of the remarkable levels of Of the 61 studies that used more than one type of biodiversity observed. The delimitation of regions, sub-molecular marker, 17 showed discordance between the regions, dominions and provinces in a continent withuniparental and biparental inherited markers. A range such a complex geological history is a challenging task.of South American organisms exhibit stronger phylo- Several authors have proposed biogeographical region-geographical structure with uniparental than biparental alization of the continent based on the identified bioticinherited markers, including algae (Tellier et al. 2009), components (as reviewed by Morrone 2006, 2010a,b).plants (Caetano et al. 2008; Collevatti et al. 2009; Palma- The complexity of the scenario can be identified by theSilva et al. 2009; Tremetsberger et al. 2009; Pinheiro et al. high variation in the number of units and subunits pro-2011), birds (Cabanne et al. 2008; Caparroz et al. 2009; posed: 98 ecoregions and six bioecoregions (DinersteinMila et al. 2009), fish (Zemlak et al. 2010) and mammals et al. 1995); 44 provinces grouped in two subrealms, 10(Culver et al. 2000; Eizirik et al. 2001; Tchaicka et al. regions and eight subregions (Rivas-Mart ınez Navar-2007; Martins et al. 2009; Hollatz et al. 2011). Possible ro 1994); 46 provinces, divided into seven subregions,reasons for discordant patterns between markers further grouped in two regions and one transition zoneinclude differences in the dispersal patterns of males (Morrone 2006); 26 provinces and six domains (Cabreraand females (Eizirik et al. 2001; Tchaicka et al. 2007; Willink 1973); 20 provinces grouped in two subre-Caparroz et al. 2009; Martins et al. 2009; Zemlak et al. gions and seven domains (Ringuelet 1975); 33 centres2010; Hollatz et al. 2011); differences between pollen vs. (M€ ller 1973); 23 domains (Ab’Saber 1977); 13 provinces u © 2012 Blackwell Publishing Ltd
  7. 7. PHYLOGEOGRAPHY OF SOUTH AMERICA 7(Fittkau et al. 1969); and two subregions (Kuschel 1969), be detailed (Antonelli Sanmartin 2011, see alsoamong others (for an extensive review, see Morrone discussion below).2006, 2010a,b). Despite some differences among the pro-posed regionalizations, there were certain concordances. Timing of phylogroup splittingFor example, most of the proposals recognized a subdi-vision between tropical and temperate portions of South An appraisal of the literature revealed emerging phylo-America, with the Neotropical biota occupying the cen- geographical patterns in the biota of South America.tre, north and east of South America and the Andean– Several studies (125) revealed the presence of deepPatagonic biota in the south and west of the continent intraspecific phylogeographical structure with multiple(Morrone 2006, 2010a,b). lineages (phylogroups). This led us to believe that many Using the simplest biogeographical subdivision of the of these could be cryptic species, that is, morphologi-214 studies in our survey, 120 (56%) were performed in cally indistinguishable (Bickford et al. 2007). However,the tropical portion of the continent, 57 (27%) in the only 13 of these studies discussed possible cases oftemperate region and 14 (6%) within the subtropical cryptic speciation (e.g. Dick et al. 2003; Camargo et Only 23 studies (11%) sampled populations 2006; Elmer et al. 2007; Fouquet et al. 2007; Morandoacross different climatic regions (Fig. 3b). Overall, our et al. 2007; Koscinski et al. 2008; Mirabello Conn 2008;review covered phylogeographical studies in several Sistrom et al. 2009; Tellier et al. 2009; Garcia et al. 2011;biomes/ecoregions of South America. Almost half of Piggott et al. 2011). Because we could not evaluatethe studies (47%) sampled only one biome/ecoregion, species’ taxonomic status to determine whether they39% sampled two or three different biomes/ecoregions were cryptic, further evaluation of the extent of thisand 13% included more than four biomes/ecoregions. phenomenon in South America is necessary.Of the latter, only one was based on plant species, an Deep phylogeographical divisions within taxa suggestextremely low number compared with those of animals extensive periods of isolation among some constituent(20 in total). The number of times that a given biome/ populations of South American species. In instances inecoregion was included in a phylogeographical study is which lineage splits have been dated, a mid-Pleistoceneshown in Fig. 5. The most studied biomes/ecoregions divergence was indicated for 57% of species (Fig. 6).were Amazonia and the Andes, which were investi- Differences in lineage splitting times were not signifi-gated in 71 and 68 studies, respectively, followed by cant with regard to climatic region: temperate, tropicalthe Brazilian Atlantic Forest (53 studies), Patagonia and subtropical (F = 0.943, P = 0.393, Table 2). Thereand Monte Desert (41 studies), Cerrado (38 studies) was, however, a significant difference in inferred split-and Chaco/Pantanal (27 studies). Gentry (1982) sug- ting time according to taxonomic group (F = 5.480;gested that the evolutionary patterns of the Amazonia P = 0.000, Table 2). Overall, mammalian, bird, fish,and Andes regions would explain much of the invertebrate and plant intraspecific phylogroups wererichness of the Neotropical domains. In fact, most structured mostly during the Pleistocene (Table S2,phylogeographical studies were concentrated in those Supporting information). In contrast, most herpetofaunaregions, and the patterns of diversification can now (amphibians and reptiles) underwent an intraspecific 80 Fig. 5 Number of times that individual biomes/ecoregions were included in a 70 phylogeographical study of South Ameri- 60 ca published between 1987 and 2011 (cat-Number of studies egories are not exclusive to a certain 50 paper, see the text for details). The corre- 40 sponding numbers of times that animals (grey) and plants (black) were addressed 30 in each biome/ecoregion are also indi- 20 cated. 10 0 on es do al o st s ga t st ó st ds er pa oc oc re oa oa an nd an in az rra es m Fo rin Ch eC eC nt at A hl m D Ce Pa Pa Ca O ig A ic te in in aH o/ nt on ar ar ac tla M M M an Ch A a/ ic fic ui ni nt G ci go tla Pa ta A Pa Biomes© 2012 Blackwell Publishing Ltd
  8. 8. 8 A. C. TURCHETTO-ZOLET ET AL. Fig. 6 Timing of lineage divergence of South American taxa based on phylogeo- graphical studies up to 2011. The bound- ary between the Quaternary and the Tertiary is placed at approximately 2.6 Ma, following Gibbard Cohen (2008). 10 00– 000 0 00 0 1. .0 2. .0 2. .6 4. .0 5. .0 6. .0 7. .0 8. .0 9. .0 10 10.0 11 11.0 12 12.0 13 13.0 14 4.0 15 15.0 16 .0 17 –17 18 18.0 19 9.0 20 20.0 21 1.0 .0 0 23 23.0 0 0 0– 00 0. 00 22 22. 4. 4. 1 2 2 4 5 6 7 8 9 6 0– 0– 0– 7– 0– 0– 0– 0– 0– –1 –1 –1 –2 –2 2 .0 .0 20. 00 0. 50 00. 0– – – – – – – – – .0 .0 .0 .0 .0 .0 .0 .0 .0 .0 .0 .0 0. 10 5 20Table 2 ANOVA of the effects of taxonomic group and climate earlier (Elmer et al. 2007). For instance, Elmer et al.region on molecular dating of intraspecific lineage diversifica- (2007), in a study of an Amazonian terrestrial leaflittertion in South America frog (Eleutherodactylus ockendeni), reported lineage split- ting from the mid-Miocene to Oligocene (20–25 Ma). General linear model The chronology of lineage splitting is important forSource of variation d.f. SS MS F P-value developing a testable hypothesis because it reveals cau- sal mechanisms and forces behind diversification pro-Taxonomic group* cesses (Rull 2011). Within the Quaternary, the main Between groups 6 872.983 145.497 5.480 0.000 environmental shifts have been linked to climatic Total 96 3262.566 changes (temperature and aridity oscillations) and theirClimate region† potential evolutionary impact on adaptability and/or Between groups 2 63.655 31.828 0.943 0.393 migration, whereas the Tertiary was characterized by Total 97 3269.173 significant tectonic and palaeogeographical reorganiza-d.f., degrees of freedom; SS, sum of squares; MS, mean square. tion leading to the creation/alteration of new pathways*Taxonomic groups: Plants; Invertebrates, Fish, Amphibian, and barriers to biotic evolution. The detection of moreReptile, Birds. Algae were not included in this analysis. ancient lineage divergences in almost half of studies†Climate region: temperate, tropical, subtropical. analysed indicates that several factors may have contributed to the geographical structure of the popula-lineage split much earlier, during the Pliocene and/or tion-level diversity of South American species. There-Miocene (Table S2, Supporting information). fore, not only Pleistocene Milankovitch cycles but also It is important to note that earlier lineage splits have earlier orogenic events (i.e. volcanic, tectonic, mountainbeen reported for a substantial amount of studies (43% uplift, alteration in drainage systems) occurring duringof the species, Fig. 6), including several taxonomic the Miocene and Pliocene likely played an importantgroups dating back to the Pliocene (fish: Ruzzante et al. role in the population divergence of South American2008; herpetofauna: Morando et al. 2008; Avila et al. 2006; species (Rull 2011).Thom et al. 2010; Noonan Gaucher 2005; Grazziotin e Students of biodiversity have discussed the relativeet al. 2006; birds: Mila et al. 2009; Chaves et al. 2007; importance of Pleistocene vs. Pliocene/Miocene eventsmammals: Eizirik et al. 2001; Hoffmann Baker 2003; in promoting the diversification of extant South Ameri-and insects: Solomon et al. 2008), to the Miocene (herpe- can species (Neotropics: Moritz et al. 2000; Bennett 2004;tofauna: Chek et al. 2001; Souza et al. 2003; Pellegrino Hewitt 1996, 2001; Rull 2006, 2008, 2011; Brunes et al. 2005; Yoke et al. 2006; Morando et al. 2007; Fitzpa- 2010; Pennington et al. 2004; Werneck et al. 2011; temper-trick et al. 2009; Guarnizo et al. 2009; Brunes et al. 2010; ate: Srsic et al. 2011). The idea that climatic oscillations eGeurgas Rodrigues 2010; Breitman et al. 2011; fish: during the Pleistocene promoted allopatric/parapatricSistrom et al. 2009; plants: Cosacov et al. 2010; Garcia speciation was the basis of the refuge theory (Hafferet al. 2011; and insects: Solomon et al. 2008) and even 1969, 2008; Prance 1973) and has been the focus of © 2012 Blackwell Publishing Ltd
  9. 9. PHYLOGEOGRAPHY OF SOUTH AMERICA 9much discussion (Bush de Oliveira 2006). What not necessarily correspond to the actual species treeseems to be evident, however, is that the marked phylo- (Pamilo Nei 1988; Avise Wollenberg 1997). More-geographical divergence documented in South Ameri- over, the inference of lineage divergence time fromcan studies is suggestive of high levels of undescribed molecular data has been criticized, mainly becausespecies diversity and a geographical structure of popu- dating is prone to many types of error (particularly forlation-level diversity. However, there is no clear overall those taxa lacking an available fossil record for calibra-pattern indicating that in South America, most species tion). Although recent improvements have increased itsoriginated during the Pleistocene, as predicted by the reliability (Rutschmann 2006; Pulquerio Nicholsrefuge theory. Instead, both Pleistocene climatic oscilla- 2007), molecular dating inferences are highly influencedtions and Pliocene/Miocene orogenic events have by calibration scheme (Sauquet et al. 2012). Hence, thecontributed to shaping the current diversity and distri- patterns we report here must be evaluated carefully. Asbution of modern species in both the Neotropical (Bush mentioned previously, further studies of multiple loci1994; Hoorn et al. 1995, 2010; Pennington et al. 2004; or using a whole-genome sequencing approach andRull 2006, 2008, 2011; Antonelli Sanmartin 2011) and increasing the intensity of geographical sampling of atemperate regions (Ruzzante et al. 2006, 2008; Mathiasen species will provide a more complete picture of the Premoli 2010; Srsic et al. 2011). e evolution and diversification of South American biota. Although formerly these explanations were consid-ered mutually exclusive, several phylogeographical Glacial vs. interglacial periodsstudies support the idea that the complex processes ofdiversification in South America were affected by the A range of phylogeographical studies in South Americainteraction of palaeogeographical and palaeoclimatic have identified multiple refugia (Table S2, Supportingforces (Bush 1994; Riddle 1996; Rull 2008). Under this information),while the contrasting pattern, demographichypothesis, many species must have begun diversifying expansion from a single refuge, was identified mainlyduring the Tertiary (Miocene/Pleistocene), perhaps as a in mammals from temperate South America (Palmaconsequence of orogenic events (i.e. Andean uplifts), et al. 2005; Rodriguez-Serrano et al. 2006; Gonzalez-Ittigachieving their current biodiversity during the Quater- et al. 2010; Lessa et al. 2010). The persistence of somenary when population structuring and young species species in multiple refugia localized throughout theiroriginated under the influence of climatic oscillations distribution indicates that these species might have(Rull 2011). For instance, in Liolaemus bibroni, a Patago- persisted through multiple climatic cycles in heteroge-nian lizard, northern and southern phylogroups neous environments. This pattern highlights the impor-diverged in the mid-Miocene (11.5 Ma), southern phylo- tance of dynamic evolutionary processes and a mosaicgroups during the Pliocene and Pleistocene (5.6–1.4 Ma) of habitats in heterogeneous landscapes that allowedand northern phylogroups in the early Pleistocene (1.5– species to persist through changing environmental con-2.3 Ma) (Morando et al. 2007). In Rhinella crucifer, a frog ditions. Accordingly, recent palaeoecological informa-species from the Brazilian Atlantic Forest, the split tion in the Neotropics indicates that during thebetween the southern and central/northern clades Quaternary, spatial reorganization and persistence inoccurred during the Pliocene (3.97 Ma), whereas splits suitable microrefugia were more frequent than completebetween the northern and central clades and within the extinctions (Vegas-Vilarrubia et al. 2011). Microrefugianorthern clades occurred during the Pleistocene (0.836 are small areas with local favourable environmentaland 0.313 Ma, respectively) (Thom et al. 2010). In e features within which small populations can surviveCalceolaria polyrhiza, a herbaceous plant species from the outside their main distribution area (the macrorefu-Andean and Patagonia regions, the northern and gium) protected from unfavourable regional environ-southern clades diverged during the late Miocene mental conditions (Rull 2009). Pollen records indicate(12.99–10.33 and 6.85–8.55 Ma, respectively). The esti- that in the southern Andes, ice-free areas might havemated time of diversification within the northern clade facilitated the maintenance of habitat refugia for forestwas also late Miocene (8.14–10.17 Ma); however, clades taxa (Markgraf et al. 1995; Heusser et al. 1999; Heussernested within the southern distribution in Patagonia 2010). In fact, the persistence of temperate southerndiverged more recently, during the Pleistocene (1.16– populations of several organisms during glacial periods1.45 Ma) (Cosacov et al. 2010). has been reported, principally plants (Muellner et al. It is important to emphasize that the patterns 2005; Marchelli Gallo 2006; Allnutt et al. 1999;reported for South America were based mostly on Azpilicueta et al. 2009; Jakob et al. 2009; Souto Premo-timing estimation procedures of a single uniparental li 2007; Tremetsberger et al. 2009; Arana et al. 2010; Co-marker (i.e. mtDNA or cpDNA; Figs 2a and 3). As dis- sacov et al. 2010; Mathiasen Premoli 2010; Premolicussed above, genealogies based on a single marker do et al. 2010; Vidal-Russell et al. 2011) and vertebrates© 2012 Blackwell Publishing Ltd
  10. 10. 10 A . C . T U R C H E T T O - Z O L E T E T A L .(fish: Zemlak et al. 2008; birds: Gonzalez Wink 2010; distribution ranges during glacial cycles. These resultsmammals: Himes et al. 2008). A number of studies highlight the importance of phylogeographical studiesshow long-term persistence of such species, including with organisms adapted to xeric habitats, which show aeven populations close to the ice-sheet coverage limit more variable response to glacial cycles than do forest-during the last glacial maximum (LGM) (Jakob et al. dwelling species. Accordingly, palaeovegetation model-2009; Cosacov et al. 2010; Vianna et al. 2011; references ling results indicate that dry tropical seasonal forests inin Srsic et al. 2011). The existence of multiple refugia e South America were fragmented during the LGM (Wer-has also been reported for other parts of the globe, neck et al. 2011), as were tropical humid forests (Carnavalwhere the effects of climatic oscillations might have Moritz 2008). Moreover, the role of glacial cycles inbeen of identical intensities to those in South America generating biotic refugia in nontropical areas of the(southern Australia: Byrne 2008; southern Europe southern hemisphere has received little attention (Behe-peninsulas: Nieto Feliner 2011; Africa: Lorenzen et al. regaray 2008; Lessa et al. 2010; Srsic et al. 2011). Because e2012). only 28% of the studies surveyed focused on species Although South American Pleistocene climate associated with open vegetation habitats, future studieschanges have been demonstrated not to be the only should focus on such organisms to better understand thedriver of speciation (e.g. Hoorn et al. 2010; Rull 2011), role of interglacial refuges in the diversification of Souththey have influenced the historical demography and American taxa (Antonelli 2008; Bennett Provan 2008;distribution of some species in South America. In fact, Werneck 2011; Werneck et al. 2011).demographic changes were identified in 58% of thestudies (Table S2, Supporting information). However, Phylogeographical breaks, colonization routes andonly a fraction (35%) of these studies included an esti- dispersal corridorsmate of the timing of such demographic oscillations.These studies suggested an important interplay between Postulating the main phylogeographical breaks, coloni-demographic scenarios and organisms associated with zation routes and dispersal corridors from the multipleforest and open vegetation habitats. A significant pro- refugia is challenging, especially considering our lim-portion of forest-dwelling species (87%, d.f. = 1, ited knowledge of the phylogeography of South Ameri-v2 = 28.69, P 0.0001) showed signs of population frag- can organisms. Generally, a complex phylogeographicalmentation during glacial cycles and/or population mosaic of patterns was observed, which was to someexpansion during interglacial periods. The geographical extent species specific. As observed in southern Euro-ranges of species associated with forest habitats were pean peninsulas (Nieto Feliner 2011), where the historyreduced mainly due to the drier conditions during of populations indicates persistence rather thanglacial cycles, which favoured the expansion of grass- complete extinction (due to drastic events), replicatedlands and savannas, following the classical model of patterns should be more scarce than in northern hemi-tropical refugia (Haffer 1969; Bennett Provan 2008), spheric regions. For instance, several studies haveas indicated by palaeovegetation reconstructions (Beh- shown how diverse ranges shift directions from theling 2002; Ledru et al. 2005). Forest species associated usual latitudinal north–south pattern. Due to thewith dry tropical forests (Caetano et al. 2008), temperate complex patterns resulting from this scenario, proposalforests (Marchelli et al. 1998, 2010; Nunez et al. 2011; of general models is difficult. However, we haveSallaberry-Pincheira et al. 2011), mountain forests attempted to summarize the most common patterns(Thom et al. 2010) and riparian forests (Marquez et al. e found.2006) accounted for 13% of studies and also indicatedpopulation expansion during interglacial periods and/ Rivers as phylogeographical barriersor fragmentation during glacial cycles. For species associated with open vegetation, the Rivers have been suggested to play an important role inpattern was unclear (v2 = 2.25, d.f. = 1, P = 0.133), as shaping biogeographical patterns in South America (Saloonly 68% of the studies showed population expansion et al. 1986; Rasanen et al. 1987; Ward et al. 2002). Theduring glacial cycles and/or fragmentation during ‘riverine’ hypothesis of diversification suggests thatinterglacial periods. Species associated with open vegeta- major rivers act as geographical barriers to dispersal oftion domains seemed to show variable responses to cli- terrestrial organisms, limiting gene flow and promotingmatic oscillations, with a tendency to expand (Marin allopatric divergence. For example, rivers within theet al. 2008; Jakob et al. 2009; Cosacov et al. 2010), to main- Amazon basin (Wallace 1852, 1876; Ayres Clutton-tain (Rodriguez-Serrano et al. 2006; Pinheiro et al. 2011; Brock 1992; Capparella 1992; Hayes Sewlal 2004) andWerneck et al. 2012) or to shrink (Gonzalez et al. 1998; Xu the Doce River in southeastern Brazil (Pellegrino et al. 2009; Gonzalez Wink 2010) their geographical 2005; Cabanne et al. 2007; Tchaicka et al. 2007; Ribeiro © 2012 Blackwell Publishing Ltd
  11. 11. P H Y L O G E O G R A P H Y O F S O U T H A M E R I C A 11et al. 2011) have been reported to be effective barriers In southern South America, other major rivers havebetween different species assemblages and populations. also been reported to act as phylogeographical breaks.Several studies have, indeed, indicated that major rivers The Plata River basin is the second largest basin inmight have acted as important phylogeographical barri- South America. The Paraguay and Plata River basinsers. The Amazon River and its tributaries are most were a significant barrier to dispersal and gene flow forfrequently reported as representing a historical barrier the cat Leopardus colocolo (Johnson et al. 1999). Theto gene flow in a range of organisms including mam- Paran River, a tributary of the Plata River basin, sepa- amals (Leopardus tigrinus: Johnson et al. 1999; Leopardus rates populations of the marsh deer Blastocerus dichoto-pardalis, Leopardus wiedii: Eizirik et al. 1998; Panthera onca: mus (Marquez et al. 2006).Eizirik et al. 2001; Callicebus lugens: Casado et al. 2007; Although the largest rivers in South America are inTapirus terrestris: De Thoisy et al. 2010; Pteronura brasili- tropical and subtropical regions, the role of severalensis: Pickles et al. 2011), birds (Xiphorhynchus spixii/ele- smaller rivers in the temperate region as potential barri-gans: Aleixo 2004; Lepidothrix coronata: Cheviron et al. ers to dispersal was examined, and structured popula-2005), insects (Charis cleonus: Hall Harvey 2002; Anoph- tions were identified. In Chile, the Maipo, Yeso andeles darling: Pedro Sallum 2009; Anophele triannulatus: Aconcagua Rivers represent major barriers to the lizardPedro et al. 2010) and frogs (Dendrobates: Symula et al. species Liolaemus monticola (Torres-Perez et al. 2007).2003). In Bol ıvia, the Magdalena River Valley was identi- The Maipo River has also been reported to be afied as a barrier to dispersal of the western and eastern geographical barrier to populations of the snake Philodr-clades of the bird Buarremon brunneinucha (Cadena et al. yas chamissonis (Sallaberry-Pincheira et al. 2011). The2007). However, the role of rivers as major drivers of Chubut River in Patagonia has affected gene flowallopatric diversification in South America has been among populations of the saxicolous mouse Phyllotischallenged by several studies that do not support the xanthopygus (Kim et al. 1998). The Chico River in Argen-riverine hypothesis (frogs and small mammals: Gascon tina was considered an ancient barrier to populations ofet al. 2000; Lougheed et al. 1999; Patton et al. 1994, 2000; the herbaceous plant Calceolaria polyrhiza (Cosacov et al.birds: Cadena et al. 2011; insects: Solomon et al. 2008; 2010) and for the reptile Liolaemus lineomaculatus (Breit-Fairley et al. 2002; and reptiles: Vasconcelos et al. 2006, man et al. 2011). More intensive geographical sampling2008). These data indicate that the population structure of an array of taxa across South America is crucial formay be an outcome of barriers that are no longer elucidation of the role of major rivers as historical barri-evident in the landscape (ancient rivers) (Lougheed et al. ers to gene flow.1999). Others have suggested a significant impact ofrecent Andean uplift on the lowlands in terms of gener- Phylogeographical patterns of freshwater organismsating the patterns of diversity along the major rivers inAmazonia (Patton et al. 1994; Gascon et al. 2000; Turner For aquatic organisms, biogeographical studies haveet al. 2004) (for ridge barriers, see discussion below). indicated the role of geographical isolation across major In southeastern Brazil, studies have pointed to the South American drainage basins in structuring and gen-Doce River basin as the phylogeographical break for erating biodiversity (as reviewed by Hubert Rennosome species (mammals: Costa 2003; lizards: Pellegrino 2006). Evidences of population genetic divergenceet al. 2005; birds: Cabanne et al. 2007, 2008; frogs: within species occupying the Amazonian River basinsThom et al. 2010; and plants: Ribeiro et al. 2011). e were observed in several fish species (PotamorrhaphisAlthough this pattern is strongly in agreement with guianensis: Lovejoy de Araujo 2000; Prochilodus magda-the historical instability involving the coastal areas lene: Turner et al. 2004; Serrasalmus rhombeus: Hubertsouth of the Doce River, as predicted by Carnaval et al. 2007; Nannostomus unifasciatus: Sistrom et al. 2009;Moritz (2008), its role as a real barrier has been Paracheirodon axelrodi: Cooke et al. 2009); turtles (Podocn-debated (Martins 2011) and even refuted (Colombi emis expansa: Pearse et al. 2006); and the Amazonianet al. 2010). Because the Doce River basin was severely River dolphin, a freshwater mammal (Inia: Banguera-affected by marine incursions during the Pleistocene, Hinestroza et al. 2002; Hollatz et al. 2011). Hollatz andthe real barrier might not have been the river itself colleagues argued that the heterogeneity of the water(Martins 2011). Additionally, contrasting topographies environment may be promoting the genetic differentia-have been evoked to explain the north/south diversity tion observed between populations on both sides of thesplit in the Doce River (Silva et al. 2012). The third Amazon River. Nevertheless, Piggott et al. (2011)largest river in South America, the S~o Franciscoa reported high population genetic differentiation, inter-River, was reported to be a geographical barrier to preted as cryptic speciation, of black-wing hatchet fishpopulations of the small rodent Calomys expulsus (Do (Carnegiella marthae) in the Rio Negro floodplain inNascimento et al. 2011). central Amazonia. An interesting finding of this study© 2012 Blackwell Publishing Ltd
  12. 12. 12 A . C . T U R C H E T T O - Z O L E T E T A L .is the cryptic speciation within a well-connected system the major drivers of biodiversity organization in Southof floodplains with no contemporary barriers that could America (Gentry 1982; Jørgensen Len-Ynez 1999; o alead population divergence. These results indicate that Antonelli et al. 2010; Hoorn et al. 2010). The Andeanthe diversity of Amazonian organisms is greatly under- Cordillera is a continuous strip that divides Southestimated. America east and west, serving as an effective moisture Rivers can have important role in influencing popula- barrier (Aragon et al. 2011). Cross-Andean disjointtion structure not only as ecological barriers but also as distributions have been reported for several organismsdispersal corridors. For instance, one study has identified (Brower 1994; Zamudio Greene 1997; Jørgensen the Casiquiare River as a dispersal corridor from the Len-Ynez 1999; Dick et al. 2003; Weigt et al. 2005; o aAmazonian to the Orinoco basins for three peacock Trenel et al. 2007; Turchetto-Zolet et al. 2012). Thesecichlid species (Cichla temensis, Cichla monoculus and patterns suggest that under the vicariance hypothesis,Cichla orinocensis: Willis et al. 2010). However, the role of lowland biota might have evolved due to Andean upliftthe geologically recent Casiquiare corridor in promoting (Gentry 1982; Raven 1999). High genetic divergencegene flow between the Amazonian and Orinoco basins between populations on either side of the Andes Cordil-has not been supported for turtle species (Podocnemis ex- lera, which suggests that differentiation is a result ofpansa: Pearse et al. 2006; Podocnemis unifilis: Escalona et al. long-term geographical isolation, has been reported for2009). several taxa including plants (Symphonia globulifera: Dick In the Guyanas coastal rivers, a divergent lineage of a et al. 2003; Dick Heuertz 2008; Cyathostegia mathewsii:freshwater fish Pseudancistrus brevispinis (Cardoso Pennington et al. 2010), birds (Lepidothrix coronata:Montoya-Burgos 2009) was identified, and the authors Cheviron et al. 2005; Adelomyia melanogenys: Chavesbelieve that sea level fluctuation during the Pleistocene et al. 2007; Glyphorynchus spirurus: Mila et al. 2009), frogscould have been responsible for this diversification. For (Rinella marina: Slade Moritz 1998; Hypsiboas andinus:the catfish Pimelodus albicans (Vergara et al. 2008), Koscinski et al. 2008), fish (Percichthys and Percilia: Ru-genetic structuring was detected among different sites zzante et al. 2006), butterflies (Heliconious erato: Browerof the Plata River basin. The populations of the fresh- 1994) and mammals (Glossophaga soricina: Ditchfieldwater catfish Trichomycterus areolatus (Unmack et al. 2000; Corollia sps: Hoffmann Baker 2003; Oreailurus2009) were highly isolated among drainage systems in jacobita: Johnson et al. 1998). These studies found geneticChile. For the Patagonian fish Galaxias platei (Zemlak population divergence across the Andes Mountainset al. 2008), the strong phylogeographical structure during a period of major Andean uplift in the Miocene,observed was influenced by both the orogeny of the in agreement with the orogeny-driven vicariancesouthern Andes and the glacial cycles of the Pleisto- hypothesis. In the wax palm plant (Ceroxylon echinula-cene. A deep phylogenetic structure was reported for tum), however, an eastern–western population splitthe Patagonian freshwater crab Aegla alacalufi (Xu et al. occurred more recently, during the Quaternary (Trenel2009). The authors believed that Pleistocene glaciations, et al. 2008). Hence, these authors propose cross-Andeandrainage isolation, habitat fragmentation and poor dispersal to be a more plausible explanation of thedispersal ability have influenced the patterns of the observed disjunction than orogeny-driven vicariance.population genetic structure of this aquatic species. In The cross-Andean dispersal hypothesis is supportedcontrast, there was little evidence of population by several other studies of aquatic and terrestrialstructure within the Paran River in the fish Prochilodus a species, including fish (Galaxias platei: Zemlak et al.lineatus (Sivasundar et al. 2001). Additionally, no phylo- 2008), small mammals (Oligoryzomys longicaudatus:geographical structure was observed by Ruzzante et al. Palma et al. 2005; Abrothrix olivaceus: Smith et al. 2001;(2011) for the Patagonian fish Percichthys trucha. This Rodriguez-Serrano et al. 2006; Dromiciops gliroides: Hi-species appears to have dispersed and mixed across mes et al. 2008; Loxodontomys micropus: Canon et al.diverse Patagonian drainages, most likely as a result of 2010; Abrothrix longipilis: Lessa et al. 2010), birds (Cyan-changes in sea level and the extension of the Patagonian oliseus patagonus: Masello et al. 2011; Adelomyia melanog-landscape that occurred during the Quaternary. enys: Chaves Smith 2011), insects (Euglossini: Dick et al. 2004) and plants (Tristerix corymbosus and Tristerix aphyllus: Amico Nickrent 2009). MigrationRidges as phylogeographical barriers across the Andean divide was possible in regionsRidges and mountain uplifts are well-known mecha- where mountains were not very high, as well asnisms of geneflow interruption and promote divergence through continuous forests (Zemlak et al. 2008; Amicoamong populations. Accordingly, evidence of this effect Nickrent 2009; Masello et al. 2011). For aquaticin a range of taxa from regions around the world is organisms, drainages that currently or previously tra-available (Soltis et al. 2006). Andean uplift was one of versed the Andes from the east side have been sug- © 2012 Blackwell Publishing Ltd
  13. 13. P H Y L O G E O G R A P H Y O F S O U T H A M E R I C A 13gested as dispersal corridors (Zemlak et al. 2008). A o/Pantanal, Caatinga, Pampas and Orinoco couldstudy of the fish Galaxias maculatus (Zemlak et al. provide important information on the demographic2010) also indicated that the Chilean Coastal Cordil- responses of populations adapted to drought stress dur-lera might represent an eastern–western dispersal bar- ing climatic oscillations because a large amount of therier. published data relates to forest-dwelling species. Hence, South America is a topographically complex conti- there is an urgent need to compile phylogeographicalnent, and although Andean uplift is one of the major studies of a wider range of taxonomic groups into aevents that contributed to biota organization, other more regionalized review of comparative phylogeogra-mountain uplifts have also been reported to have acted phy of important South American regions. This willas phylogeographical barriers to South American spe- facilitate more accurate elucidation of phylogeograph-cies. For example, the Serra do Mar and Mantiqueira ical patterns and promote a better understanding of themountain uplifts in southeastern Brazil for a freshwater origin and maintenance of South American biota.turtle during the Pliocene and Miocene (Hydromedusamaximiliani: Souza et al. 2003), for rats (Trinomys: Lara AcknowledgementsPatton 2000) and freshwater fish (Mimagoniates microl-epis: Torres Ribeiro 2009). The Mitaraka archipelago We thank three anonymous referees for valuable comments oninselbergs, in French Guiana, represent a strong barrier the manuscript. This work was supported by grants to CP-S from CNPq (Universal: 471775/2010-0) and FAPESP (Biota:to gene flow among Pitcairnia geyskesii populations 2009/52725-3; 2009/17411-8), to FP from FAPESP (2010/15052-0),(Boisselier-Dubayle et al. 2010). to ACTZ from PNPD/CAPES-FAPERGS fellowship and FAPERGS (Pronex: 10/0028-7).Conclusions and future perspectivesAn increasing number of studies of South American Referencesphylogeography have recently been published. None- Ab’Saber AN (1977) Os domnios morfoclimticos na Amrica ı a etheless, the number remains insufficient, pointing to an do Sul: primeira aproximac~o. Geomorfologia, 53, 1–23. ßaurgent need for more investigations of historical bioge- Acosta MC, Premoli AC (2010) Evidence of chloroplast captureography and phylogeography to assess how species in South American Nothofagus (subgenus Nothofagus, Notho-responded to past changes and to predict how they fagaceae). Molecular Phylogenetics and Evolution, 54, 235–242. 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Journal of Ornithology, 148,the Brazilian Atlantic Forest (Martins 2011; Porto et al. S443–S453.2012; Silva et al. 2012), plants from Pampas grassland Allnutt TR, Newton AC, Lara A et al. (1999) Genetic variation(Fregonezi et al. 2012) and tetrapods from the Amazonia in Fitzroya cupressoides (alerce), a threatened South Americanregion (Aleixo Rossetti 2007; Antonelli et al. 2010). It conifer. Molecular Ecology, 8, 975– important to highlight the fact that most of these Amico GC, Nickrent DL (2009) Population structure andrecent reviews discuss mainly vertebrate patterns, likely phylogeography of the mistletoes Tristerix corymbosus and T. aphyllus (Loranthaceae) using chloroplast DNA sequence var-because this taxonomic category is the most studied in iation. American Journal of Botany, 96, 1571–1580.South America (89% of phylogeographcial studies). In Antonelli A (2008) Higher level phylogeny and evolutionaryaddition, a greater number of plant (trees and herbs) trends in Campanulaceae subfam. Lobelioideae: molecularand invertebrate species, which show contrasting signal overshadows morphology. Molecular Phylogenetics anddispersal abilities, should be included to generate a Evolution, 46, 1–18.nonbiased picture of biota evolution in South America. Antonelli A, Sanmartin I (2011) Why are there so many plantWe predict that in the next few years, next-generation species in the Neotropics? Taxon, 60, 403–414. Antonelli JA, Quijada-Mascare~ as A, Crawford JA, Bates JM, nsequencing techniques will solve most of the problems Velazco PM, Wuster W (2010) Molecular studies and paleo-encountered in plant groups due to the low diversity of geography of Amazonian tetrapods and their relation to geo-molecular markers, thus facilitating phylogeographical logical and climatic models. In: Amazonia, Landscape andstudies of a broader range of organisms. Phylogeo- Species Evolution (eds Hoorn C, Wesselingh F), pp. 386–404.graphical studies of the xeric regions of Cerrado, Chac- Wiley-Blackwell.© 2012 Blackwell Publishing Ltd