Journal of Biogeography (J. Biogeogr.) (2013) 40, 905–914 ORIGINAL Dispersal and vicariance of ARTICLE malabaricus (Bloch, 1794) (Teleostei, ) 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 , 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, State, 2 populations of were subject to the same geomorphological , 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 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, , 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. 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 to Buenos Aires (34–29° S), characterized by the presence of Oligosarcus jen- in (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 Laguna dos Patos (30–34° S). River Basin, in the Parana´/ 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., 1998, 2002; Lemos et al., 2002; confluence of adjacent rivers and allow freshwater fish to dis- Vicari et al., 2005, 2006; Santos et al., 2009). In northern perse among basins. During interglacial periods, high sea lev- populations, H. malabaricus from the coastal basins of the els engulf the lower part of drainage systems, resulting in and Contas rivers share the same karyomorph vicariance of obligatory freshwater fish (Weitzman et al., (40F) with most populations from the Sa˜o Francisco Basin 1988; Beheregaray et al., 2002). The sea-level variation (Bertollo et al., 2000; Jacobina et al., 2009), and some from hypothesis is supported by the existence of extensive and the eastern Amazon (Bertollo et al., 2000).

906 Journal of Biogeography 40, 905–914 ª 2012 Blackwell Publishing Ltd Phylogeography of Hoplias malabaricus on the Brazilian coast

Currently, there are no plausible hypotheses to explain chromosomal speciation models (reviewed in Rieseberg, karyotypic divergence within this species complex. Bertollo 2001). Although the local dynamics of chromosome rear- et al. (2000) indicate that karyomorphs do not exchange rangement fixation processes may be easily blurred by multi- genetic material in sympatric conditions; therefore karyotypic ple vicariance and dispersal events in the Neotropical region characters are a reliable tool to assess lineage distinctiveness (Albert & Reis, 2011), the apparent substitution of kar- or speciation within H. malabaricus. Although we agree with yomorph 42A by its closely related 42B in the Doce River Faria & Navarro (2010) that there is little evidence to sup- Basin (Santos et al., 2009; Jacobina et al., 2011) suggests that port early models of chromosome speciation, circumstantial chromosomal rearrangements may involve selective advanta- evidence suggests that demographic factors affect the likeli- ges (Kirkpatrick & Barton, 2006). hood of fixation of chromosome rearrangements. Within the The aim of this study was to test the effects of the Erythrinidae, levels of karyotypic variation are apparently proposed endemism regions on the molecular divergence correlated with ecological traits that allow species to survive patterns of H. malabaricus karyomorphs in Brazilian coastal in different with presumably different population river basins and to discuss geomorphological scenarios sizes. The species group includes large fishes consistent with these patterns. adapted to open, well-oxygenated waters (Rantin et al., 1992) and their large populations are characterized by a sta- MATERIALS AND METHODS ble karyotype of 2n = 50 chromosomes (Morelli et al., 2007). The H. malabaricus species group is better adapted to less Samples of H. malabaricus were collected from 18 river oxygenated waters (Rantin et al., 1992), lives in isolated pop- basins on the Brazilian coast, including the Sa˜o Francisco ulations and has seven karyotypes. Continuous, facultative Basin, some smaller basins collectively known as the Brazilian air breathers of the genera and Eastern Basin, and minor coastal basins of south-eastern (Graham, 1997) have five and four karyomorphs respectively, Brazil (Table 1, Fig. 1a). Hoplias intermedius was used as the and show even larger levels of chromosome variation (Diniz outgroup. DNA was extracted from ethanol-fixed tissue & Bertollo, 2006; Morelli et al., 2007). This familial pattern samples (liver, epaxial muscle or gill filaments) according to is consistent with at least three demography-dependent Dergam et al. (2002). Collecting permit SISBIO14975-1 was

Table 1 Hoplias malabaricus samples, acronyms, geographical coordinates and collection localities on the Brazilian coast.

Hydrographical basin Acronym GPS coordinates Locality

Sa˜o Francisco SA03; SA04; SA09; SA20; S18° 43′ 52″ W44° 22′ 30″ Das Velhas River, Curvelo, MG SA25; SA29; SA35; SA56; Paraguac¸u EE67 S 12° 34′ 56″ W39° 00′ 00″ Pedra do Cavalo Dam, Gov. Mangabeira, BA Contas PC03; PC08 S 13° 52′ 22″ W40° 03′ 39″ Das Contas River, Jequie´,BA Jequitinhonha AA101 S 16° 56′ 33″ W42° 00′ 49″ Calhauzinho River, Arac¸uaı´,MG EE01; EE02 S 16º 50′ 58′’W41º 47′ 07′’Sa˜o Marcos, Arac¸uaı´,MG MT01 S 16° 34′ 06″ W41° 28′ 00″ Itaobim, MG Jucurussu JD675 S 16° 36′ 21″ W40° 28′ 04″ Jucurussu River, Palmo´polis, MG Buranhe´m JD698; JD701 S 16° 24′ 48″ W39° 35′ 13″ Buranhe´m River, Euna´polis, BA JD668 S 16° 57′ 54″ W40° 30′ 42″ River, Palmo´polis, MG Itanhe´m JR01 S 17 ° 32′ 07″ W39° 13′ 52″ Alcobac¸a River, , BA JD654 S 17 ° 04′ 30″ W40° 47′ 55″ Itanhe´m River, between A´ guas Formosas and Machacalis, MG JD580 S 17° 48′ 33″ W40° 27′ 42″ Mucuri River, Nanuque, ES JD637 S 17° 02′ 12″ W40° 57′ 49″ A´ guas Formosas, MG Sa˜o Mateus JD506 S 18° 45′ 31″ W40° 38′ 17″ Muniz River, ES JD465 S 18° 44′ 21″ W40° 53′ 29″ Sa˜o Mateus River, ES JD550; JD546 S 18° 43′ 43″ W39° 46′ 33″ Preto River, ES Doce PF12 S 19° 46′ 32″ W42° 35′ 22″ Dom Helvecio Lake, Marlie´ria, MG PF28; PF33 S 19° 45′ 30″ W42° 37′ 02″ Carioca Lake, Marlie´ria, MG Itabapoana CT614; CT617 S 21° 08′ 09″ W41° 39′ 31″ Bom Jesus do Itabapoana, RJ Paraı´ba do Sul JD1225 S 21° 04′ 88″ W42° 20′ 53″ Muriae´ River, Muriae´,MG CT666 S 21° 29′ 79″ W42° 31′ 45″ Sr. Alair Valverde de Magdaleno, MG Macae´ JD3876 S 22° 29′ 35″ W42° 13′ 35″ Macae´ River, Casimiro de Abreu, RJ Sa˜o Joa˜o CT690; CT691 S 22° 40′ 54′’W42° 22′ 19′’ D’Ouro River, Silva Jardim, RJ Macacu MN04 S 22° 25′ 17″ W42° 37′ 40″ Macacu Waterfalls, RJ Ribeira de Iguape IG03 S 24° 29′ 11″ W47° 50′ 30″ Ribeira River, SP Ilha do Cardoso AD08; AD09 S 23° 10′ 13′’W47° 58′ 49′’ Cardoso Island, SP Perequeˆ OH03 S 25° 22′ 50″ W48° 27′ 01″ Perequeˆ River, Paranagua´,PR

Journal of Biogeography 40, 905–914 907 ª 2012 Blackwell Publishing Ltd T. L. Pereira et al.

(a)

(b)

(c)

Figure 1 Phylogeography of Hoplias malabaricus. (a) Study area along the Brazilian coast and topology generated using fragments of (b) mitochondrial ATPase-6 and (c) nuclear RAG2. Statistical support generated with posterior probability (Bayesian inference) and bootstrap (parsimony). * denotes polytomy branches. The bar represents the molecular distance. issued to J.A.D. by the National Institute Chico Mendes of product was used in a 10-lL cycle sequencing reaction using Biodiversity (ICMBio); this authorization is valid for the col- a dRhodamine terminator cycle sequencing kit (PE Applied lection of all fish taxa in Brazil. Voucher specimens were Biosystems, Carlsbad, CA, USA). For RAG2, PCR conditions deposited in the Museu de Zoologia Joa˜o Moojen at the were as follows: 95 °C (5 min), 30 cycles of 95 °C (30 s), Universidade Federal de Vic¸osa, Vic¸osa, Minas Gerais State, 48 °C (45 s), and 72 °C (1.5 min), with a final extension at Brazil. 72 °C for 7 min. The PCR products were purified using PEG The ATP synthase 6 (ATPase-6) gene was amplified with 8000 (20% polyethyleneglycol, 2.5 M NaCl) and sequencing primers L8524 and H9236 (Quenouille et al., 2004). A frag- was performed on a Macrogen sequencing platform (Macro- ment of recombination activating gene 2 (RAG2) was ampli- gen, Seoul, South Korea). fied in 12 H. malabaricus samples using the primers RAG2aF Sequences were aligned using Clustal W (Higgins et al., and RAG2bR (Lovejoy & Collette, 2001). For both reactions, 1994) implemented in mega 5.0 (Tamura et al., 2011). DNA was synthesized in 50-lL reactions containing 0.4 lL Bayesian inference (Huelsenbeck & Ronquist, 2001) was per- of dNTPs (20 mm), 5 lL of reaction buffer (200 mm Tris- formed for ten million Markov chain Monte Carlo (MCMC)

HCl, pH 8.4, 500 mm KCl), 0.4 lL of MgCl2 (100 mm), trees using four chains with default priors. The molecular 2 lL of each primer (10 mm), 0.4 lL (2.5 U) of Taq DNA evolution models that best fit the data were chosen using polymerase (Phoneutria), 2 lL of template DNA (100 ng/ MrModeltest 2 (Nylander, 2004) and the mean distances lL) and 37.8 lLofH2O. For ATPase-6, polymerase chain within and among clades were estimated using the selected reaction (PCR) conditions were as follows: 94 °C (2 min), models in mega 5.0 (Tamura et al., 2011). The first 25% of five cycles of 94 °C (45 s), 54 °C (45 s) and 72 °C (1.5 min), generations were discarded as burn-in, and the phylogeny and 29 cycles of 94 °C (45 s), 58 °C (45 s) and 72 °C and posterior probabilities were estimated from the remain- (1.5 min). PCR products were purified using Qiaquick (Qia- ing trees. Topologies with posterior probabilities equal to gen Inc., Valencia, CA, USA); 5 lL of the purified PCR or greater than 0.95 were considered to be well supported

908 Journal of Biogeography 40, 905–914 ª 2012 Blackwell Publishing Ltd Phylogeography of Hoplias malabaricus on the Brazilian coast

(Wilcox et al., 2002). Maximum parsimony analyses were morph (J.A.D., unpublished data). The molecular distance carried out with paup* 4.0b10 (Swofford, 2002). Heuristic for haplotypes within the Eastern A haplogroup was lower searches consisting of 1000 random addition sequences were than that observed within the Eastern B haplogroup performed using the tree bisection–reconnection (TBR) (Table 2). The Southeastern haplogroup included the south- branch-swapping algorithm. The phylogenetic signal was ernmost populations of trahiras from the Ribeira, Paranagua´ assessed using 1000 standard bootstrap pseudoreplicates and Macacu rivers, as well as the Cardoso Island samples. (Felsenstein, 1985). Topologies with bootstrap values higher Except for the latter population, whose karyotype is than 95 were considered to be well supported. Sequences unknown, all other populations share 2n = 42 chromosomes were deposited in GenBank (accession numbers: GQ848614– (J.A.D., unpublished data). This haplogroup was also charac- GQ848618, GQ848625–GQ848642, JX848698–JX848728). terized by very low internal genetic distance (Table 2). Alignment of RAG2 sequences yielded 1239 bp with 42 variable sites, 15 phylogenetically informative sites and a 5.25 RESULTS transition/transversion ratio, which suggested a lack of satu- Sequence alignment of the 676-bp ATPase-6 fragment yielded ration. The data fitted the K80 model. Sequences were 180 variable and 146 parsimony informative sites. The transi- grouped into three well-supported (Bayesian) or two well- tion/transversion ratio was 6.4, suggesting that substitution supported (parsimony) clades. The first clade was congruent rates were not saturated. The best molecular evolution model with the Northeastern haplogroup, the second included was TN93 + G. Both Bayesian and parsimony methods the Eastern A and B haplogroups, and the third clade indicated that the same four haplogroups were congruent represented the Southeastern haplogroup. This cladogram is with the geographical distribution of the populations, with fully consistent with the diploid number of the specimens high posterior probability and bootstrap values (Fig. 1b), and the geographical distribution of the populations and high molecular distance among them (Table 2). These (Fig. 1c). Low molecular divergence was observed within the clades were labelled as the Northeastern, Eastern A, Eastern 42-chromosome clade of H. malabaricus (0.001), whereas B, and Southeastern haplogroups. molecular divergence was eleven times higher between the The Northeastern haplogroup was composed of popula- 2n = 40 and 2n = 42 chromosome clades (0.011). tions from the Sa˜o Francisco Basin and some coastal rivers, characterized by 2n = 40 chromosomes (Jacobina et al., DISCUSSION 2009), the so-called 40F karyomorph (Bertollo et al., 2000). Within-sequence divergence was highest in this haplogroup The haplogroups identified by ATPase-6 sequence alignment (Table 2), with three well-supported subhaplogroups that were congruent with geomorphological sections of the Brazil- included closely related haplotypes from the Jequitinhonha/ ian coast (Cruz et al., 1985). This suggests that the vicariance Buranhe´m, Contas/Jequitinhonha/Paraguac¸u and Sa˜o Fran- of this species was directly driven by palaeohydrographical cisco/Contas/Buranhe´m/Jequitinhonha rivers. The Eastern A processes involving complex tectonic, geomorphological, cli- haplogroup was composed of two well-supported popula- matic and active oceanographical events. tions (Bayesian posterior probabilities) or one well-supported The Northeastern haplogroup was composed of H. mala- haplogroup (parsimony). Under Bayesian analysis, these two baricus populations from the Sa˜o Francisco River Basin and subhaplogroups were composed of haplotypes from the coastal basins where sea cliffs have been carved from Forma- Mucuri/Sa˜o Mateus/Doce and Jucurussu/Itanhe´m rivers, c¸a˜o sandstone reef sediments, and from organic reef respectively; these populations share 2n = 42 chromosomes constructions. Likewise, the coastal regions for Eastern A and (Born & Bertollo, 2001; Jacobina et al., 2011). Likewise, the B haplogroups were clearly divided by geological structures. Eastern B haplogroup included two well-supported haplo- The Eastern A haplogroup populations were distributed groups (Bayesian analysis) or one well-supported haplogroup north of the mouth of the Rio Doce, an area of beach ridges, (parsimony). According to the Bayesian results, the two sub- deltas, sea cliffs and sandstone reefs. The Eastern B haplo- haplogroups were composed of populations from the Itpab- group was distributed over a region spanning from Paraı´ba apoana/Paraı´ba do Sul and Paraı´ba do Sul/Sa˜o Joa˜o/Macae´ do Sul to the Cabo Frio Magmatic Lineament, a region char- rivers; again, these populations all share the 2n = 42 karyo- acterized by rocky coasts, barrier lagoons and mangrove

Table 2 Molecular distance using ATPase-6 sequencing and Bayesian estimates for divergence times with 95% confidence intervals in Hoplias malabaricus from the Brazilian coast. Values above the diagonal represent the distance between haplogroups. Values on the diagonal represent the distance within haplogroups.

Northeastern haplogroup Eastern haplogroup A Eastern haplogroup B Southeastern haplogroup

Northeastern haplogroup 0.025 0.087 0.111 0.108 Eastern haplogroup A 0.005 0.068 0.087 Eastern haplogroup B 0.009 0.095 Southeastern haplogroup 0.007

Journal of Biogeography 40, 905–914 909 ª 2012 Blackwell Publishing Ltd T. L. Pereira et al. swamps. The Southeastern haplogroup occurred south of Nematocharax (, one species) and Wertheimeria Cabo Frio, in a region isolated by the Serra do Mar relief (Doradidae, one species). In addition to affecting freshwater and characterized by a granite-gneiss crystalline basement ichthyofauna, the emergence of the Abrolhos Formation dur- (Villwock et al., 2005). ing interglacial periods was associated with a dry climate and The Northeastern haplogroup suggests faunal dispersal the local formation of hypersaline lagoons. These ecological events involving coastal rivers and the Sa˜o Francisco River conditions are suggested by the presence of carbonates and Basin. These patterns were consistent with the ‘Pattern C’ the scarcity of fluvial sediments in the interior southern hypothesis (Ribeiro, 2006), which includes stream piracy range of the Abrolhos Formation. These local conditions may between coastal and crystalline Brazilian shield rivers. Plio- have reinforced vicariance, affecting distribution patterns of cene geomorphological data suggest the Sa˜o Francisco River terrestrial contemporary biota, including semi-deciduous for- tributaries in the Arac¸uaı´ region (Minas Gerais State) were est tree species (Santos et al., 2011) and lizards (Pellegrino captured by the Jequitinhonha River (Saadi, 1995) due to et al., 2005). Neogenic reactivation of the Taiobeiras Fault, with east–west The east coast of Brazil is characterized by a large number movements that defined the current eastern border of the of relatively small rivers, sometimes flowing in close proxim- northern Serra do Espinhac¸o Mountains (Saadi et al., 2002). ity, and limited to the west by the Serra do Mar and Serra This pattern suggests a Sa˜o Francisco Basin origin for the do Espinhac¸o reliefs. In this region, molecular and cytoge- Jequitinhonha (EE02) and Buranhe´m (JD668) haplotypes. netic data suggest that H. malabaricus populations are more The subhaplogroup that included the Jequitinhonha affected by glaciation-related sea level cycles than by stream (AA101), Paraguac¸u (EE67) and Contas (PC08) haplotypes piracy between coastal rivers and the continental Sa˜o Fran- probably dispersed more recently from the Sa˜o Francisco cisco Basin. On the other hand, stream capture among these Basin. An even more recent dispersal would explain close coastal basins may also explain their close genetic similarities. phylogenetic relatedness between the Contas (PC03), Bathymetric surveys north of the mouth of the Doce River Buranhe´m (JD701 and JD698) and Jequitinhonha (EE01 and show that various channels converge on the Abrolhos depres- MT01) and Sa˜o Francisco Basin haplotypes. Faunal similarity sion. Depressions are delimited by the current isobath of between the latter two basins is further suggested by the 60 m and surrounded by high topographies that reach the occurrence of endemic Acinocheirodon melanogramma, which 30 m isobath (Kowsmann & Costa, 1979). The Pleistocene occurs only in these drainage systems (Malabarba & Weitz- lagoons are delimited to the south by the mouth of the Doce man, 1999). Northeastern Brazilian coastal basins are isolated River and to the north by the Abrolhos Formation. The close and apparently strongly influenced by two processes: stream phylogenetic relationship between the Itanhe´m and Jucurussu piracy from the Sa˜o Francisco basin and sea level fluctua- haplotypes supports a more recent common palaeohydrologi- tions at their lower portions. cal history involving basins within this region. Some coastal The north-eastern H. malabaricus populations occur north freshwater fish (Astyanax taeniatus, Corydoras nattereri, of the Abrolhos Formation, a notable enlargement in the Hyphessobrycon bifasciatus, Mimagoniates microlepis and continental shelf that forms two submerged coastal protru- Trachelyopterus striatulus) also reach the northern limit of sions between 17° and 20° S arising from the development their distribution range in the Mucuri and Jucuruc¸u rivers. of coral banks and sedimentary rocks on the volcanic sub- In addition, the monophyletic genera Microcambeva (Trich- strate. These continental shelf protrusions are also referred to omycteridae, two species), Mimagoniates (Characidae, six as the Abrolhos and Royal Charlotte banks and are 246 km species), Pogonopoma (Loricariidae, three species), Scleromys- and 110 km wide, respectively, at their most extreme points tax (Callichthyidae, five species) and Spintherobolus (Characi- (Guazelli & Carvalho, 1981). This bank complex has an esti- dae, four species) are all endemic to the coastal systems mated age of 59–37 Ma (Eocene) and must have functioned south of the Abrolhos Formation. as a physical barrier to ichthyofauna of the Northeastern and Although the H. malabaricus populations from the Eastern Eastern haplogroups. Bathymetric features of the continental A and Eastern B haplogroups both have 2n = 42 chromosomes shelf in Abrolhos include high topographical peaks associated (Jacobina et al., 2011), molecular data indicate no evidence of with palaeodrainage carved by Pleistocenic fluvial activity genetic exchange between the Doce and Paraı´ba do Sul rivers (Kowsmann & Costa, 1979). For example, exposure of the during glacial periods. Within the Eastern B haplogroup, the continental shelf at the end of the Wisconsin Regression two subhaplogroups (Itabapoana/Paraı´ba do Sul and Macae´/ (21,000 years ago) can be inferred by accentuated iron oxide Sa˜o Joa˜o/Paraı´ba do Sul rivers) suggest independent dispersal pigmentation in neighbouring coastal sediments. In the events between the hydrographical basins to the north and Abrolhos Bank, bathymetric depressions reflect environmen- south of the Paraı´ba do Sul. To the south, molecular data sug- tal changes caused by the Flandrian Depression (14–7 Ma). gest a relevant vicariant effect of the Cabo Frio Magmatic Line- These data are congruent with fish fauna endemic to the ament (Riccomini et al., 2005), which isolated the eastern and coastal systems north of the Abrolhos Formation, such as the south-eastern coastal basins during glacial periods. This mag- Copionodontinae subfamily (, five species) matic alignment was formed from groups of alkaline igneous and the monophyletic genera Kolpotocheirodon (Characidae, rocks from the Late Cretaceous and Palaeogene, which have two species), Acinocheirodon (Characidae, one species), structural features developed from Jaboticabal (Sa˜o Paulo

910 Journal of Biogeography 40, 905–914 ª 2012 Blackwell Publishing Ltd Phylogeography of Hoplias malabaricus on the Brazilian coast

State) eastwards up to the border between continental and Molecular results indicated that two non-exclusive oceanic crusts (Riccomini et al., 2005). processes shaped the evolution and diversification of coastal The topology generated using RAG2 and the greater populations of Hoplias malabaricus, and presumably affected molecular distance between trahiras with 40 and 42 chromo- patterns of endemism of other fish. The first process was rep- somes indicated that the 2n = 42 populations of the coastal resented by sea level variation. During glacial periods, low sea basins south of the Abrolhos Bank are monophyletic. levels prompted confluence of rivers within geomorphological Nuclear RAG2 has a lower rate of substitution (Lovejoy & sections of the Brazilian coast, while the Abrolhos Formation Collette, 2001) and seems suitable for the reconstruction of and Cabo Frio Magmatic Lineament promoted vicariance deep phylogenies (Javonillo et al., 2010). The base rate of among north-eastern, eastern and south-eastern populations. ATPase-6 substitutions is higher and therefore did not The second process was stream piracy involving continental resolve the coalescence of the four haplogroups. Based on and coastal drainage systems, as observed in the Northeastern this gene, Santos et al. (2009) proposed paraphyly of the 42A haplogroup, or stream piracy between coastal drainages, as karyomorphs within the H. malabaricus species complex. suggested by the O. acutirostris distribution range. The occurrence of two main groups of karyomorphs to the north and south of the Abrolhos Formation should be ACKNOWLEDGEMENTS interpreted in the wider context of South American biogeog- raphy. Karyomorphs 40F and 42A are not sister clades and This work was supported by the Conselho Nacional de Desen- are more related to Amazon/Surinam and Parana river basin volvimento Cientı´fico e Tecnolo´gico (CNPq), Coordenac¸a˜ode populations, respectively. Based on chromosome morphol- Aperfeic¸oamento de Pessoal de Nı´vel Superior (CAPES) and ogy, Bertollo et al. (2000) suggest the 40F karyomorph is Fundac¸a˜o de Amparo a Pesquisa do Estado de Minas Gerais closely related to the 40/41G karyomorph, which occurs in (FAPEMIG). We thank Paulo L.S. Carneiro and Claudio M. the Amazonian Aripuana˜ and Trombetas drainages. The 40F Volcker for the collection of specimens and Nicholas Walker karyomorph also occurs in north-eastern Brazil and in the for revision of the English manuscript. Tocantins River in the State of Para´ (Bertollo et al., 2000). On the other hand, the 42A karyomorph is widely repre- REFERENCES sented in the Upper and Lower Parana´, reaching southern basins in Uruguay and Argentina (Bertollo et al., 2000). Abell, R., Thieme, M.L., Revenga, C. et al. 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