Dispersal and Vicariance of Hoplias Malabaricus
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Journal of Biogeography (J. Biogeogr.) (2013) 40, 905–914 Hoplias ORIGINAL Dispersal and vicariance of ARTICLE malabaricus (Bloch, 1794) (Teleostei, Erythrinidae) populations of the Brazilian continental margin Tiago L. Pereira1, Udson Santos1*, Carlos E. Schaefer2, Gisele O. Souza1, Samuel R. Paiva3, Luiz R. Malabarba4, Eduardo E. Schmidt1 and Jorge A. Dergam1 1Departamento de Biologia Animal, Campus ABSTRACT Universita´rio, Universidade Federal de Vic¸osa, Aim The aim of this study was to test the hypothesis that the Brazilian coastal 36570-000, Vic¸osa, Minas Gerais State, 2 populations of Hoplias malabaricus were subject to the same geomorphological Brazil, Departamento de Solos, Campus Universita´rio, Universidade Federal de Vic¸osa, and palaeohydrological factors that resulted in endemic fish regions, by charac- 36570-000, Vic¸osa, Minas Gerais State, terizing the mitochondrial DNA, nuclear sequences and cytogenetic data of Brazil, 3Laborato´rio Gene´tica Animal, Parque these populations. Estac¸a˜o Biolo´gica, Embrapa Recursos Location Seventeen coastal basins in north-eastern, eastern and south-eastern Gene´ticos e Biotecnologia, 70770-900, Brası´lia, Brazil, plus the Sa˜o Francisco Basin. Distrito Federal, Brazil, 4Departamento de Zoologia, Campus Universita´rio, Universidade Methods Forty-two specimens were analysed. Mitochondrial ATP synthase 6 Federal do Rio Grande do Sul, 91501-970, (ATPase-6) and nuclear recombination activating gene 2 (RAG2) gene Porto Alegre, Rio Grande do Sul State, Brazil sequences were used for Bayesian inference and maximum parsimony analyses. Molecular models were selected using MrModeltest. Results Molecular analyses indicated four haplogroups (Northeastern, Eastern A, Eastern B and Southeastern) for ATPase-6 and three clades for RAG2. All topologies were congruent with Hoplias malabaricus diploid numbers, with most regions of proposed endemism and coastal geomorphological units. Main conclusions Deep genetic divergence between the Northeastern and the other haplogroups was interpreted as evidence of the vicariant effect of the Abrolhos Formation, which effectively isolates 2n = 40 and 2n = 42 coastal populations. To the south, the Cabo Frio Magmatic Lineament also isolates the Eastern and Southeastern 2n = 42 populations. In the Northeastern haplo- group, stream piracy was probably involved in chronologically varied dispersal events between coastal and continental basins. All haplogroups also included haplotypes that dispersed in recent times. Results show an older vicariant pattern and recent dispersal events congruent with the occurrence of temporary connections along the coast caused by eustatic sea level variations and the occurrence of stream piracy involving either continental or coastal basins, and suggest these processes contributed to the current distribution patterns of *Correspondence: Udson Santos, Departamento de Biologia Animal, Av. P.H. Brazilian coastal freshwater fish. á Rolfs s/n, Campus Universit rio, Universidade Keywords Federal de Vic¸osa, 36570-000, Vic¸osa, Minas Gerais State, Brazil. Biogeography, biogeographical units, Brazil, coastal basins, freshwater fish, E-mail: [email protected] Neogene, phylogeography, Sa˜o Francisco Basin. restricted to aquatic environments, they are excellent indica- INTRODUCTION tors for studies of past palaeohydrology and environmental The Neotropical freshwater fish fauna has long been consid- changes. Related forms of freshwater fish can only occur in ered the richest in the world (Bo¨hlke et al., 1978; Schaefer, isolated basins in which there was a connection to 1998; Albert & Reis, 2011). Because freshwater fish are other water bodies in the past. Distribution patterns of ª 2012 Blackwell Publishing Ltd http://wileyonlinelibrary.com/journal/jbi 905 doi:10.1111/jbi.12044 T. L. Pereira et al. monophyletic taxa can be used to generate hypotheses that complex fluvial systems now submerged under the ocean may be tested using non-related aquatic organisms, and a gen- (e.g. Suguio et al., 1985; Justus, 1990; Abreu & Calliari, 2005; eral concordance of these patterns may indicate a common Menezes et al., 2008; Buckup, 2011). Additionally, stream history for the region (Nelson & Platnick, 1981). Neotropical piracy between coastal basins (Saadi, 1995) may explain fish distribution patterns were the subject of many early faunal similarities. papers (e.g. Ihering, 1891; Eigenmann, 1909; Haseman, 1912; The shared occurrence of related species in coastal and Menezes, 1972; Weitzman et al., 1988) and molecular continental drainages was interpreted as the outcome of tec- approaches have recently been added to these analyses (e.g. tonic events that promoted stream piracy among drainages Hubert et al., 2007; Willis et al., 2010; Albert & Reis, 2011). (Ribeiro, 2006). In the eastern coastal region of Brazil, this Within the Neotropics, the eastern coastal river basins of hypothesis explains the occurrence of the same taxa in drain- Brazil have traditionally been considered a biogeographical ages that are currently isolated by the Serra do Mar Relief, unit because of their high numbers of endemic genera and resulting in a high degree of recent faunal dispersal (the species (Vari, 1988; Weitzman et al., 1988; Bizerril, 1994; ‘C pattern’ proposed by Ribeiro, 2006). Two additional, older Buckup, 2011). Whereas some taxa are typically restricted to patterns were proposed by Ribeiro (2006): the ‘B pattern’ asso- small sets of basins or to a single drainage system (e.g. spe- ciated with Tertiary cladogenetic events and the ‘A pattern’ cies of Crenicichla, Deuterodon, Epactionotus, Hollandichthys, involving Cretaceous vicariant events. Lignobrycon, Microcambeva, Mimagoniates, Pogonopoma, Scle- In addition to comparing faunal composition among river romystax, Spintherobolus and Trichogenes), some species are basins, the geological evolution of coastal and continental widely distributed (e.g. Mimagoniates microlepis and Hoplias basins may also be explored through phylogeographical anal- malabaricus). ysis of widespread species, especially using genetically-based Studies of species distribution patterns along the Brazilian characters such as mitochondrial DNA (Avise et al., 1992), Atlantic coastal drainages resulted in partially coincidental nuclear DNA (Wilson & Veraguth, 2010), and cytogenetic proposals to subdivide regions of endemism. Menezes (1988) data. Sedentary species are particularly suitable for studies of proposed three regions: a Northern region from the Doce phylogeographical patterns because low levels of gene flow River (19° S) to the mouth of the Jequitinhonha River (16° favour genetic differentiation between populations. This is S), where Oligosarcus acutirostris (his ‘species C’) occurs; a the case for the trahira, Hoplias malabaricus (Bloch, 1794) Central region ranging from the Cubata˜o River (27° S) to (Teleostei, Erythrinidae), one of the most widely distributed the Itabapoana River (21° S) to the north, characterized by Neotropical characiforms, which occurs in the cis-Andean the occurrence of Oligosarcus hepsetus; and a Southern region region from the Pacific coast of Costa Rica to Buenos Aires (34–29° S), characterized by the presence of Oligosarcus jen- in Argentina (Berra, 2007). This species is a sedentary ynsii and Oligosarcus robustus. Bizerril (1994) proposed bottom dweller (Kalinin et al., 1993) and its distribution Southeast and East coastal subprovinces, based on 285 spe- overlaps the range of its family (Oyakawa, 2003). cies ranges between the mouth of the Sa˜o Francisco River Since the seminal studies of Bertollo et al. (1978, 1979), (10° S) to the north and 29° S to the south, which roughly H. malabaricus has been considered a species complex, charac- coincide with Menezes’ (1988) Central and Southern subdivi- terized by high levels of karyotypical variation (Bertollo et al., sions. Carvalho (2007) conducted a parsimony and ende- 2000). There are currently seven recognized karyomorphs that mism analysis on distribution data of 145 freshwater fish vary in diploid number, chromosome morphology and the taxa and proposed the North (10–17° S), East (17° S – 22° presence of sex chromosome systems (Bertollo et al., 2000; S), Southeastern (22–28° S), and South (28–32° S) drainage Santos et al., 2009) and we followed their nomenclature. groups. Finally, Abell et al. (2008) classified the Atlantic Most populations in coastal basins of south-eastern Brazil drainages into six ecoregions based on species compositions have a diploid number of 42 chromosomes, usually with no at different taxonomic levels: Northeastern Atlantic Forest sex chromosome system (karyomorph 42A), except in the (10–21° S), Paraiba do Sul (21–22° S), Fluminense (22° S), Doce River Basin where the 42B karyomorph with an XX/XY Ribeira de Iguape (23–24° S), Southeastern Atlantic Forest system is prevalent (Born & Bertollo, 2001; Jacobina et al., (24° S – 29° S), Tramandaı´-Mampituba (29–30° S), and 2011). The 2n = 42A karyomorph also occurs in the Uruguay Laguna dos Patos (30–34° S). River Basin, in the Parana´/Paraguay drainage system and in The occurrence of related species in Brazilian Atlantic the Amazon Basin (Born & Bertollo, 2001). Molecular and coastal basins has been ascribed to the effects of sea level cytogenetic data indicate that at least some coastal popula- variations caused by glaciation cycles (Weitzman et al., tions are related to other populations in the continental 1988). During glacial maxima, low sea levels may favour Parana´ Basin (Dergam et al.,