Cladistic biogeography of the Neotropical region: identifying themain events in the diversification of the terrestrial biota

Juan J. Morrone*

Departamento de Biologa Evolutiva, Museo de Zoologa Alfonso L. Herrera, Facultad de Ciencias, Universidad Nacional Autonoma de Mexico

(UNAM), Mexico, DF, Mexico

Accepted 29 April 2013

Abstract

A cladistic biogeographical analysis was undertaken to identify the main events in the biotic diversification of the terrestrial

Neotropical biota. For the 36 animal and plant taxa analysed, a component 9 area matrix was constructed, associating geo-

graphical data only with informative nodes, and it was analysed under implied weights using the software TNT. The general

area cladogram obtained shows that the Neotropical region constitutes a monophyletic unit, with a first split separating the

Antilles and a second one dividing the continental areas into a north-western and a south-eastern component. Within the north-

western component the areas split following the sequence northern Amazonia, south-western Amazonia, north-western South

America, and Mesoamerica. Within the south-eastern component the areas split following the sequence south-eastern Amazonia,

Chaco, and Parana. The three main components are treated as subregions: Antillean, Amazonian (northern Amazonian, south-

western Amazonian, Mesoamerican, and north-western South American dominions), and Chacoan (south-eastern Amazonian,

Chacoan, and Parana dominions). Dispersal and vicariant events postulated to explain these pattens might have occurred during

the Cretaceous, when the Caribbean plate collided with the Americas, a combination of eustatic sea-level changes and tectonic

deformations of the continental platform exposed large parts of South America to episodes of marine transgressions, and the

Andean uplift reconfigured the Amazonian area. Tertiary and Quaternary events are assumed to have later induced the diversifi-

cation within these large biogeographical units.

The Willi Hennig Society 2013.

The tropics of the Americas are well known for theirremarkable biodiversity, which is due to habitat heter-ogeneity and a complex geological history, both beingresponsible for the patterns of geographical distribu-tion of species and clades. Forests are among the mostcommon Neotropical biomes, particularly the Amazonforest, but there are also extensive open biomes, e.g.the diagonal of South America comprising the Pampa,Chaco, Cerrado, and Caatinga. One of the firsthypotheses to account for the diversification of theAmazonian terrestrial biota was provided by Wallace(1852), who considered that the rivers from the Ama-zon basin have acted in the past as barriers to dis-persal. An alternative explanation, the Pleistocene

refugia theory, postulated that the Amazonian forestwas fragmented through Pleistocenic climatic changes,resulting in an archipelago of patches or refuges (Haf-fer, 1969, 1974, 1997; Vanzolini and Williams, 1970;Prance, 1982; Lourenco, 1986). Some authors havesince postulated that Pleistocene climatic changes havenot been arid enough to fragment the forest and thatvicariance was caused by the formation of islands inelevated areas (Colinvaux et al., 1996, 2000; Colinv-aux, 1997, 1998; Colinvaux and Oliveira, 1999) andothers even invalidated the existence of refugia by con-sidering them to be sampling artefacts (Nelson et al.,2009). Other authors postulated that more ancient,pre-Quaternary vicariant events explained general pat-terns of distribution of Amazonian taxa (Croizat,1958, 1976; Cracraft and Prum, 1988; Bush, 1994; Pat-ton et al., 2000; Amorim, 2001; Nihei and Carvalho,

*Corresponding author:

E-mail address: juanmorrone2001@yahoo.com.mx

Cladistics

Cladistics 30 (2014) 202214

10.1111/cla.12039

The Willi Hennig Society 2013

2004, 2007; Jaramillo et al., 2006; Rull, 2008; Hoornet al., 2010). The open biomes have been also analysedrecently (Ramos and Melo, 2010; Werneck, 2011), buttheir integration with analyses of the areas with forestbiomes is rare (e.g. Sigrist and Carvalho, 2009; Piresand Marinoni, 2010; Costa, 2003).The formal definition of the Neotropical region

began in the 19th century. De Candolle (1820) did notrecognize the Neotropical region, but he listed fiveregions that correspond to it: Mexico, tropical Amer-ica, Chile, southern Brazil and Argentina, and Tierradel Fuego. Sclater (1858), based on bird taxa, dividedthe world into six zoogeographical regions; and Wal-lace (1876) later accepted this scheme, applying it toother vertebrate taxa. According to the SclaterWal-lace system, the Neotropical region comprises Southand Central America, reaching as far north as centralMexico. This scheme has been largely accepted eversince, especially by zoogeographers working with ver-tebrates (Cox, 2001). Several biogeographers workingwith plants or with invertebrates, however, haveadopted a more restrictive definition of the Neotropi-cal region, excluding the southern portion of SouthAmerica, because of its closest links to Australia, NewGuinea, and New Zealand (Engler, 1879, 1882; Drude,1884; Gill, 1885; Allen, 1892; Lydekker, 1896; Diels,1908; Monros, 1958; Kuschel, 1964; Cabrera and Wil-link, 1973; Good, 1974; Takhtajan, 1988; Amorim andTozoni, 1994; Morrone, 2002a; Moreira-Mu~noz,2007). In this restricted sense, the Neotropical regioncorresponds to the tropics of the New World, i.e.,most of South America, Central America, southernMexico, the West Indies, and southern Florida (Mor-rone, 2006; p. 477), explicitly excluding the Andeanarea of South America, which is assigned to theAndean region, and northern Mexico, which isassigned to the Nearctic region. The Mexican Transi-tion zone represents the overlap between the Nearcticand Neotropical regions, whereas the South AmericanTransition zone represents the overlap between theNeotropical and Andean regions (Morrone, 2006,2010a). If both transition zones are included within it,we have the Neotropical region sensu lato, and if theyare not included, the Neotropical region sensu stricto(Fig. 1).Regarding the biogeographical regionalization of

the Neotropical region, there have been several pro-posals recognizing subregions or dominions within it(Sanchez Oses and Perez-Hernandez, 1998; Morrone,2010b). Wallace (1876) identified four subregions:Mexican (southern Mexico and Central America),Antillean (West Indies), Brazilian (tropical SouthAmerica), and Chilean (southern or temperate SouthAmerica). Cabrera and Willink (1973) recognized fivedominions: Caribbean (Mexico and the Antilles),Amazonian, Guyanan, Chacoan, and Andean-Patago-

nian. For South America, several authors have recog-nized two subregions: one named Guyano-Brazilianor Brazilian, and the other named Andean-Patago-nian, Patagonian, Argentinean, Chilean, or Austral(Cabrera and Yepes, 1940; Ringuelet, 1961, 1975; Fit-tkau, 1969; Hershkovitz, 1969; Kuschel, 1969; Sick,1969; Smith, 1983; Rivas-Martnez and Navarro,1994; Almiron et al., 1997; Kreft and Jetz, 2010;Proches and Ramdhani, 2012). This main divisionwithin South America has been also evidenced byecogeographical (Bailey, 1998) and macroecologicalanalyses (Ruggiero et al., 1998; Ruggiero andEzcurra, 2003). Morrone (2001) proposed a classifica-tion of the Neotropical region, based on panbiogeo-graphical analyses, dividing it into four subregions:Caribbean, Amazonian, Chacoan, and Parana. Mor-rone and Coscaron (1996) undertook a parsimonyanalysis of endemicity based on South American Pei-ratinae (Heteroptera: Reduviidae), hypothesizing thatthe gradual development of an open vegetation diago-nalcomprising the Chaco, Cerrado, and Caatingaseparated a former forest into a north-western part(north-western South America and Amazonian forest)and a south-eastern part (Parana and Atlantic

Fig. 1. The Neotropical region, with the Mexican and South Ameri-

can transition zones represented by dashed lines. The Neotropical

region sensu stricto does not include these transition zones, whereas

the Neotropical region sensu lato encompasses them.

J. J. Morrone / Cladistics 30 (2014) 202214 203

forests). This hypothesis was corroborated by a cla-distic biogeographical analysis (Morrone and Co-scaron, 1998). Other cladistic biogeographical analyses(Amorim, 2001; Nihei and Carvalho, 2007; Sigristand Carvalho, 2009; Pires and Marinoni, 2010;Echeverry and Morrone, in press) have questionedthe naturalness of the Amazonian and Caribbeansubregions of Morrone (2006).My objective is to analyse the relationships of differ-

ent areas of the Neotropical region to test its natural-ness, revise its regionalization, and identify the mainevents in the biotic diversification of the terrestrialNeotropical biota.

Material and methods

Areas

I analysed eight areas (Fig. 2), which have beenidentified as biogeographical units in previous studies(Rapoport, 1968; Savage, 1982; Amorim and Pires,1996; Amorim, 2001; Morrone, 2001, 2006 Nihei andCarvalho, 2007; Ramos and Melo, 2010; Echeverryand Morrone, in press). The Caribbean and Amazo-nian subregions, as previously recognized (Morrone,2006), were divided into three smaller units each totest their naturalness. The eight areas analysed are asfollows:1 Mesoamerica: lowlands of southern and central

Mexico and most of Central America (Guatemala,Belize, Honduras, El Salvador, and northern Nicara-gua).2 Antilles: West Indies (Bahamas, Greater Antilles,

and Lesser Antilles).3 North-western South America: western Ecuador

and Colombia, north-western Venezuela, Panama,Costa Rica, and southern Nicaragua.4 Northern Amazonia: Amazonian forest, basically

north of the Amazon river.5 South-eastern Amazonia: Amazonian forest,

south-east of the Amazon river.6 South-western Amazonia: Amazonian forest,

south-west of the Amazon river.7 Chaco: open vegetation areas in northern and

central Argentina, southern Bolivia, western and cen-tral Paraguay, Uruguay, and central and north-easternBrazil.8 Parana: forests from north-eastern Argentina,

eastern Paraguay, southern Brazil (west of the Serrado Mar and toward central Rio Grande do Sul), andeastern Brazil.Additionally, four external areas were included to

test the naturalness of the Neotropical region: theNearctic and Andean regions, and the Mexican andSouth American transition zones (Morrone, 2006).

Taxa

Thirty-six taxa (Table 1) were analysed. Theyinclude genera and species groups of insects, spiders,vertebrates, and plants, which were chosen becausephylogenetic hypotheses were available for them andtheir species are distributed in the areas analysedherein. Although there are other potential taxa withpublished phylogenetic analyses that could be consid-ered, some of them lack information on the geographi-cal distribution of the species analysed and othersinclude only a limited sample of the terminal taxa, asoccurs in most molecular analyses. Some of the taxaanalysed herein have been considered in previous cla-distic biogeographical studies (Morrone and Coscaron,1998; Nihei and Carvalho, 2007; Sigrist and Carvalho,2009; Pires and Marinoni, 2010; Echeverry and Mor-rone, in press).

Analysis

A cladistic biogeographical analysis is based on acorrespondence between phylogenetic relationships

Fig. 2. Units of the analysis. (a) Nearctic region; (b) Mexican Tran-

sition Zone; (c) Mesoamerica; (d) Antilles; (e) north-western South

America; (f) northern Amazonia; (g) south-eastern Amazonia; (h)

south-western Amazonia; (i) Chaco; (j) Parana; (k) South American

Transition Zone; (l) Andean region.

204 J. J. Morrone / Cladistics 30 (2014) 202214

and area relationships (Morrone, 2005a, 2009; Parentiand Ebach, 2009). It comprises three basic steps: (1)construction of taxonarea cladograms from taxoncladograms, by replacing the terminal taxa by thearea(s) inhabited by them; (2) resolution of the prob-lems due to widespread taxa, redundant distributionsand missing areas; and (3) derivation of general areacladogram(s) representing the most logical solutionfor all the taxa analysed (Morrone and Carpenter,1994). General area cladograms represent hypotheseson the biogeographical history of the taxa analysedand the areas where they are distributed (Morrone,2009).

To obtain the general area cladogram(s), a parsi-mony analysis of paralogy-free subtrees (Nelson andLadiges, 1996; Contreras-Medina et al., 2007; LeonPaniagua and Morrone, 2009; Morrone, 2009) wasundertaken. This method consists of four steps(Fig. 3):1 For each taxonarea cladogram, areas duplicated

or redundant in the descendants of a node are elimi-nated (Fig. 3a), so that geographical paralogy is elimi-nated or reduced significantly, and data are associatedonly with informative nodes.2 Components are identified on each of the paralo-

gy-free subtrees obtained (Fig. 3b).

Table 1

Taxa analysed, with the paralogy-free subtree derived from them

Taxa Paralogy-free subtrees Reference(s)

Insecta: Coleoptera

Agaporomorphus Fig. 4a Miller (2001)

Chroaptomus Fig. 4b Chani-Posse (2006)

Entinmini Fig. 4c,d Morrone (2002b), Vanin and Gaiger (2005)

Hypselotropis Fig. 4eg Mermudes (2005)

Ptychoderes Fig. 4h,i Mermudes and Napp (2006)

Rhinostomus Fig. 4j Morrone and Cuevas (2002)

Insecta: Diptera

Coenopsia Fig. 4k Nihei and Carvalho (2004)

Polietina Fig. 4l Nihei and Carvalho (2007)

Pseudoptilolepis Fig. 4m Schuehli and Carvalho (2005)

Sepedonea Fig. 4n Pires and Marinoni (2010)

Insecta: Hemiptera

Eidmannia Fig. 4o Coscaron (1989), Morrone and Coscaron (1998)

Nicomia Fig. 4p Albertson and Dietrich (2005)

Rasahus Fig. 4q,r Morrone and Coscaron (1998)

Rhodnius Fig. 4s,t Paula et al. (2007)

Serdia Fig. 4u,v Fortes and Grazia (2005)

Thoreyella and related genera Fig. 4w Bernardes et al. (2009)

Insecta: Lepidoptera

Amorbia Fig. 4xz, aa Phillips-Rodrguez and Powell (2007)

Charis gynaea species group Fig. 4bb Hall and Harvey (2001)

Cliniodes Fig. 4ccff Hayden (2011)

Insecta: Orthoptera

Abracrini Fig. 4ggii Da Costa et al. (2010)

Arachnida: Araneae

Anelosinus ethicus species group Fig. 4jj Agnarsson (2005)

Vertebrata: Aves

Amazona ochrocephala complex Fig. 4kk Eberhard and Bermingham (2004)

Chlorospingus ophthalmicus species complex Fig. 4ll Bonaccorso et al. (2008)

Pionopsitta Fig. 4mm Ribas et al. (2005)

Vertebrata: Mammalia

Alouatta Fig. 4nn Cortes-Ortiz et al. (2003)

Ateles Fig. 4oo Collins and Dubach (2000)

Caluromys Fig. 4pp Costa (2003)

Marmosa murina Fig. 4qq Costa (2003)

Metachirus nudicaudatus Fig. 4rr Costa (2003)

Oryzomys megacephalus species group Fig. 4ss Costa (2003)

Rhipidomys Fig. 4tt Costa (2003)

Plants

Exostema Fig. 4uu McDowell et al. (2003)

Hillia Fig. 4vvxx Taylor (1994)

Prosopis Fig. 4yy, zz Catalano et al. (2008)

Sabal Fig. 4aaa Zona (1990)

Stigmatopteris Fig. 4bbb, ccc Moran (1991)

J. J. Morrone / Cladistics 30 (2014) 202214 205

3 A data matrix is compiled, scoring with 1 thepresence of a component in an area and 0 itsabsence (Fig. 3c).4 A parsimony analysis of the data matrix is under-

taken to identify the general area cladogram (Fig. 3d).Analysis of the 36 taxonarea cladograms identified

55 paralogy-free subtrees (Fig. 4), 85 informative com-ponents were extracted from them, and a data matrixwas constructed (Table 2). The matrix was analysedusing TNT (Goloboff et al., 2008), performingsearches of the most parsimonious cladograms withthe heuristic traditional search algorithm of TNT,with 1000 replications, and tree-bisection-reconnectionbranch-swapping (TBR), holding ten trees during eachreplication. The effect of homoplasy on the results wasexplored by conducting different implied weights anal-yses (Goloboff, 1993), with constants of concavity (k)set to a different integer value of 130, where 1 isweighted most severely against homoplastic characters.

Results

Two most parsimonious cladograms were obtainedanalysing the matrix under equal weights. Impliedweights calculated with different constants of concav-ity (k = 130) consistently produced one of them(Fig. 5). This general area cladogram shows that the

Neotropical areas in the strict sense constitute a mono-phyletic unit, whereas the Mexican and South Ameri-can transition zones are the sister areas to the Nearcticand Andean regions, respectively. Within the Neotrop-ical region in the strict sense, a first dichotomy sepa-rates the Antilles from the continental areas, which ina second dichotomy are arranged into a north-westernand a south-eastern component. Within the north-wes-tern component the areas split according to thesequence northern Amazonia, south-western Amazo-nia, north-western South America, and Mesoamerica.Within the south-eastern component the areas split fol-lowing the sequence south-eastern Amazonia, Chaco,and Parana. According to these results, the Caribbeanand Amazonian subregions as formerly recognized byMorrone (2006) under a panbiogeographical frame-work do not represent natural areas: within the for-mer, the Antilles do not group with Mesoamerica andnorth-western South America; and within the latter,south-eastern Amazonia is closer to Chaco and Paranathan to the remaining Amazonian areas.Based on the general area cladogram, the following

regionalization is proposed:Neotropical regionAntillean subregionAmazonian subregionNorthern Amazonian dominionSouth-western Amazonian dominion

(a)

(b)

(c) (d)

Fig. 3. Steps of the cladistic biogeographical analysis. (a) Original taxonarea cladograms; (b) paralogy-free subtrees derived from the taxon

area cladograms, with informative components marked on them; (c) data matrix of areas 9 components; (d) general area cladogram obtained.

206 J. J. Morrone / Cladistics 30 (2014) 202214

Mesoamerican dominionNorth-western South American dominion

Chacoan subregionSouth-eastern Amazonian dominionChacoan dominionParana dominion

Some of the events implied by the general area clad-ogram (Fig. 6) can be associated with known tectonicand geological information available:1 The oldest event corresponds to the former

connection between the North American and SouthAmerican landmasses during the Early Jurassic to

(a)

(h)

(m)

(n)

(u)

(z) (aa)(bb)

(ee) (ff)(gg)

(hh)

(nn)

(ss)

(xx)(yy) (zz)

(aaa)

(bbb)(ccc)

(tt) (uu)(vv)

(ww)

(oo)

(pp)(qq)

(rr)

(ii) (jj) (kk) (mm)(ll)

(cc)

(dd)

(v)(w)

(x) (y)

(o) (p) (q)(r)

(s)

(i)

(j) (k)

(l)

(b)(c)

(d) (e) (f) (g)

Fig. 4. Paralogy-free subtrees analysed. (a) Agaporomorphus; (b) Chroaptomus; (c,d) Entimini; (eg) Hypselotropis; (h, i) Ptychoderes; (j) Rhino-

stomus; (k) Coenopsia; (l) Polietina; (m) Pseudoptilolepis; (n) Sepedonea; (o) Eidmannia; (p) Nicomia; (q,r) Rasahus; (s,t) Rhodnius; (u,v) Serdia;

(w) Thoreyella and related genera; (xz, aa) Amorbia; (bb) Charis gynaea species group; (ccff) Cliniodes; (ggii) Abracrini; (jj) Anelosinus ethicus

species group; (kk) Amazona ochrocephala complex; (ll) Chlorospingus ophthalmicus complex; (mm) Pionopsitta; (nn) Alouatta; (oo) Ateles; (pp)

Caluromys; (qq) Marmosa murina; (rr) Metachirus nudicaudatus; (ss) Oryzomys megacephalus species group; (tt) Rhipidomys; (uu) Exostema; (vv

xx) Hillia; (yy, zz) Prosopis; (aaa) Sabal; (bbb, ccc) Stigmatopteris. Areas as in Fig. 2.

J. J. Morrone / Cladistics 30 (2014) 202214 207

Table 2

Data matrix, where files correspond to the areas analysed and columns to the components identified in the paralogy-free subtrees of Fig. 4

root

00000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000

Nearctic region

00000000000000000000001000011111011000000000000000000000000000001001000000000000000011101000000000000000000000000000000000000000000000000000011111000000000

Mexican Transition Zone

00111000000000000000001000011111010000000000000000000000000000101000000000000000000000000000000000000000000000000000000000000000001111111000000000000000000

Mesoamerica

00111010000000010100101111111110011111100000001000000110010000110001111110001111011011111100000000100101000100000110100000000000001111111001100111111111111

Antilles

00000000000000000000001111100000000000000000000000000000000000001100001000001100010100000000000000000000000000000000000000000000000000000101100111101000010

North-western South America

00110000000110000110001100011100011100110100101111000111010000001111111111111000010111001111010100110111110111110110100000000000000001110111000111111111111

Northern Amazonia

00000011010111000000111110011000000000110110110011111001100000001111100011101110000000000001100010111001101111100100000100101111001001110100000000001110000

South-eastern Amazonia

10000000000001111111111111000000011100000000000010000000000000001110000000000000000000000001100000000001101110001111011111001111110000000100000000000000000

South-western Amazonia

11100111011101100111111111011000000000000011000000011000011000001111101011111110000011010001110100111111110111110111000110111001101001000111000110001111000

Chaco

11000011100000011111001111010000111110111000000011110000000111001110000011111111100000001111111011000000000111000000010000001110001110000000011110000000000

Parana

11100111111000011111110111110000111111111011111111111001100111111110001111001111111010010001111011000000000110001000011111111101110001100100000000001100000

South American Transition Zone

00000000000000000000000000000000000000000000000000011100011100000000000000000000000000000000000000000000000000000000000000000000001100000000010100000000000

Andean region

00000000000000000000000000000000000000000000000000000000000110000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000000

208

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Early Cretaceous (190148 Ma). It allowed the geodis-persal of the Neotropical biota to North America andwould explain the presence of ancient Neotropical ele-ments in northern Mexico (Halffter, 1987; Morrone,2005b).

2 The vicariance between the Antilles and the restof the Neotropical region can be linked to the sever-ance of the temporal connection represented by theleading edge the Caribbean plate during its north-east-ward drift (Echeverry and Morrone, in press). The

Fig. 5. General area cladogram obtained.

(a) (b) (c)

(d) (e) (f)

(g) (h)Fig. 6. Sequence of events implied by the general area cladogram. (a) Geodispersal of the Neotropical biota from South to North America; (b)

vicariance of the Antilles and the rest of the Neotropical region; (c) vicariance of the north-western and south-eastern continental components;

(d) vicariance of northern Amazonia and the rest of the north-western component; (e) vicariance of south-western Amazonia and north-western

South AmericaMesoamerica; (f) vicariance of north-western South America and Mesoamerica; (g) vicariance of southern Amazonia and Chaco-

Parana; (h) vicariance of Chaco and Parana.

J. J. Morrone / Cladistics 30 (2014) 202214 209

leading edge of the Caribbean plate reconnected tem-porarily with North and South America at 125100 Ma. This connection began to be severed in theLate Cretaceous (80 Ma) and finished in the Mioceneto Middle Pliocene (Pitman et al., 1993). The conti-nental mainland constituting the rest of the Neotropi-cal region shares extensive hydrological connectionsand there is evidence that it constituted a superbasinthat has persisted in relative isolation since at least theLate Cretaceous (Albert et al., 2011).3 The vicariance between the north-western and

south-eastern continental components of the Neotropi-cal region might have begun with the formation of alake along the Amazon, Madeira, and Mamore rivers,in the Late Cretaceous; and finished with the forma-tion of a wide epicontinental sea by water invasionthrough the north, east, and south portal seaways, inthe Miocene (Amorim, 2001; Frailey, 2002; Nihei andCarvalho, 2004, 2007).4 The vicariance between northern Amazonia and

the remaining areas of the north-western continentalcomponent can be linked to the Romeral Fault Zoneand/or the final uplift of the northern Andes. TheRomeral Fault, of Cretaceous age, is an active andcontinuous fault system almost 700 km long that com-prises three or four parallel regional faults, which formthe boundary between autochthonous continentalrocks to the east and accreted oceanic arc rocksrelated to Caribbean terranes in the west (Kennan andPindell, 2009; Heads, 2012; Echeverry and Morrone,in press). The uplift of the Andes began in the Creta-ceous, but has been more conspicuous since the Mio-cene, 237 Ma, and finished in the Pliocene (Lundberget al., 1998; Kennan, 2000; Cortes-Ortiz et al., 2003;Garzione et al., 2008; Hoorn et al., 2010).5 The vicariance between south-western Amazonia

and north-western South AmericaMesoamerica canbe linked to the formation of an epicontinental sea bywater invasion through the Maracaibo and Amazonbasins in the Pliocene (Rodrguez-Olarte et al., 2011).6 The vicariance between Chaco and Parana can be

linked to the connection of the Parnaba and Paranabasins in the Palaeocene (Amorim, 2001; Nihei andCarvalho, 2004).

Discussion

Previous analyses have suggested that the Amazo-nian and Caribbean subregions might not be naturalareas. Amorim and Pires (1996) considered thatAmazonia consisted of two non-related areas: north-western Amazonia and south-eastern Amazonia. Amo-rim (2001) also considered that the Amazon forest didnot correspond to a natural biogeographical area,being geographically delimited, based on the Amazon

river basin. Costa (2003) undertook a comparativephylogeographical analysis of forest-dwelling smallmammals distributed between and within the Amazonand Atlantic forests, finding that sequence similaritywas often greater between samples from the AtlanticForest and either Amazon or central Brazilian foreststhan it was within each of both forest areas. TheAtlantic Forest clades were either not reciprocallymonophyletic or were the sister group to all the otherclades, and the central Brazilian area did not behaveas a separate region but as complementary to eitherthe Amazon or the Atlantic forests. Nihei and Carv-alho (2007) tested two previous proposals (Amorimand Pires, 1996; Morrone, 2006), by undertaking dif-ferent cladistic biogeographical analyses based on theareas implied by these authors, and concluded thatAmazonia should be regarded as a composite area,because north-western Amazonia was closely related tothe Caribbean subregion, whereas south-easternAmazonia was related to the Chacoan and Paranasubregions. Sigrist and Carvalho (2009) analysed thehistorical relationships among Neotropical areas ofendemism using Brooks parsimony analysis (BPA) toexamine whether the inclusion of open area formationsinfluences area relationships of the surrounding forests.They found a basal split between the Amazonian andAtlantic forests, suggesting that they have been iso-lated for a long period of time, and corroborated thehypothesis that Amazonia is a composite area; how-ever, when they added two areas with open formations(Cerrado and Caatinga), internal relationships withinAmazonia changed, so they concluded that a biogeo-graphical classification comprising both forests andopen formations should be preferred given their com-plementary history. Pires and Marinoni (2010) appliedBPA to species of Sepedonea (Diptera: Sciomyzidae),finding that when the Cerrado and Caatinga wereincluded the Atlantic forest was monophyletic, whereasthe Amazonian forest was not, and concluded that asingle history of the current distribution of taxa in thearea analysed was unlikely. A recent panbiogeographi-calcladistic biogeographical analysis of the Caribbeansubregion based on plant and animal taxa (Echeverryand Morrone, in press) showed that it is not a naturalarea. Differences among these analyses may be due todifferent delimitations of the areas of endemism,absence of non-forested areas in most of the analyses,and the fact that most analyses did not use testableprocedures (Sigrist and Carvalho, 2009).The major events postulated herein might have

occurred during the Cretaceous, when the Caribbeanplate collided with the Americas (Echeverry et al.,2012), a combination of eustatic sea-level changes andtectonic deformations of the continental platformexposed large parts of South America to episodes ofmarine transgressions (Albert and Reis, 2011), and

210 J. J. Morrone / Cladistics 30 (2014) 202214

Andean uplift reconfigured the Amazonian area (Gar-zione et al., 2008; Hoorn et al., 2010). Tertiary andQuaternary events are assumed to have induced thediversification within these large biogeographical units(Bush, 1994; Werneck, 2011). The vicariance betweenthe Antilles and the rest of the Neotropical region,and the vicariance between the north-western andsouth-eastern continental components are coincidentwith previous cladistic biogeographical analyses (Amo-rim and Pires, 1996; Amorim, 2001; Nihei and Carv-alho, 2004). The dispersal of the Neotropical biotafrom South to North Americaa prerequisite for thefirst vicariant eventhas been supported by severalauthors, working on different taxa, who have previ-ously recognized two cenocrons: Old Southern orAncient Neotropical that dispersed between the Cre-taceous and the Palaeocene; and a younger one thatdispersed between the Pliocene and Pleistocene, afterthe establishment of the Panama Isthmus (Rosen,1976; Gentry, 1982; Savage, 1982; Bussing, 1985;Halffter, 1987; Morrone, 2005b). It is interesting tonote that the vicariance between north-western SouthAmerica and Mesoamerica occurs more recently thandetected in some previous analyses (Amorim and Pires,1996; Amorim, 2001; Camargo and Pedro, 2003),where it was considered as an older vicariant event. Inthe present analysis this event has a younger age, assuggested by Camargo (1996) and Camargo and Mo-ure (1996).Several authors (Bush, 1994; Bates et al., 1998;

Marks et al., 2002; Costa, 2003; Nihei and Carvalho,2007) have concluded that it is not possible to postu-late a single hypothesis explaining the current distribu-tion of the Neotropical terrestrial biota. Pires andMarinoni (2010) have even suggested that in theabsence of temporal information (inferred from molec-ular phylogenies) one cannot be sure that a generalpattern is due to a common history of biotic diversifi-cation. Additionally, it might be argued that taxashowing so different dispersal means may not show aclear, congruent pattern. I think, however, that biogeo-graphical regionalizations are useful as general refer-ence models (Ribichich, 2002). Their heuristic valueshould be explored by examining the geographical dis-tribution of other plant and animal taxa. Molecularphylogenetic analyses that have been calibrated mayallow us to disprove the proposed sequence of vicari-ant events and help to clarify the time frame of theevents that led to the biotic diversification of the Neo-tropics.

Acknowledgments

I thank Amparo Echeverry and Dalton de SouzaAmorim for interesting discussions on the biogeogra-

phy of the Neotropics. Amparo Echeverry, MichaelHeads, and two anonymous reviewers made usefulcomments that helped improve the manuscript.

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