Generalized additive model
The strongest marine BGF and hence the location of maximum phylogeographic concordant genetic discontinuities along the Brazilian coast was Natal, at central Rio Grande do Norte. Natal, is located 51 km south of Cape São Roque, the easternmost promontory of the South American continent, and the region where the South American continent turns southward at 05° S latitude. Cape São Roque is also where the broad offshore SEC end up bifurcating into two nearshore boundary currents, the northward North Brazil Current and the southward Brazil Current (Molinari, 1983; R. Peterson & Stramma, 1991). Most likely, this largest BGF concordance along the Brazilian coast is related to the bifurcation of the SEC at this region of the coast. The split of nearshore boundary currents has been recognized as a common vicariant biogeographic process promoting genetic discontinuities in continuously distributed marine species, including species with high dispersal capabilities (Avise, 2000). Examples include the oysterCrassostera virginica and the red alga Gracilaria tikvahiae distributed north and south of Cape Canaveral where the northward Gulf Stream is deflected offshore and southward costal currents arrive from northern latitudes (Gurgel, Fredencq, & Norris, 2004; Reeb & Avise, 1990). Phylogeographic Region I is also recognized as the region with overall larger values in the frequency of BGF concordances for other sites along the Brazilian coast. This region is characterized by a tropical climate, with wet winters and dry summers, strong coastal winds, nearshore sedimentary reefs and higher tidal amplitudes compared to the other regions of Brazil’s coastline. Most of the SEC flows into the strong North Brazil Current and hence offshore transport within this current is considered higher (R. Peterson & Stramma, 1991).
The flow in opposite directions of the two Brazilian boundary currents was first proposed as a BGF in the phylogeographical study of the crustacean Micropogonias furnieri (Puchnick-Legat & Levy, 2006). Since then several other studies have tested and detected BGF at this region, including another crustacean (Panulirus argus: Diniz, Maclean, Ogawa, Cintra, & Bentzen, 2005), six fish species (Bezerra et al., 2018; Cortinhas et al., 2016; da Silva et al., 2016; Mendonça, Oliveira, Gadig, & Foresti, 2011; Montes et al., 2018; Santos et al., 2006), some plant species (Rhizophora spp.: Francisco, Mori, Alves, Tambarussi, & de Souza, 2018; Pil et al., 2011), and a turtle species (Eretmochelys imbricata: Proietti et al., 2014). Our results therefore identify the split of the SEC as the main process driving producing the greatest pattern of BGF overall concordance along the Brazilian coast, answering one of the main questions in this study.
Phylogeographic Region II (10° S – 20.5° S) represents the coastline influenced by the first half of the Brazil Current. The transport of the Brazil Current, and hence its connectivity capabilities, is weak throughout its southward flow compared to other boundary currents because most of the water mass from the SEC is diverted northward into the North Brazil Current (R. Peterson & Stramma, 1991). Within Region II coastal counter-currents and other historical, geographical, climatic, estuarine and oceanographic processes play important roles driving marine larval dispersal and genetic connectivity (da Silva et al., 2016; Imron et al., 2007; Pil et al., 2011). Region II, presents a relative constant value in the frequency of potential BGF occurrences averaging at 19% from Ipoiuca (8° 33’ S) to the Abrolhos Reef Basin and the Vitória-Trindade seamount chain at latitude 20.5° S. BGF within this region are considered weak, porous, intermittent or species-specific, with strong influence on the distribution of several marine organisms (da Silva et al., 2016). Along this coastline, potential BGF are traditionally associated with the mouth of large rivers such as the São Francisco, the Paraguaçu, and the Doce. River-associated vicariance in Brazil was first proposed for terrestrial lizards (Pellegrino et al., 2005) and then observed for others marine taxa, such as the mollusksAnomalocardia brasiliana (Arruda, Beasley, Vallinoto, Marques-Silva, & Tagliaro, 2009) and the fish Rhizoprionodon porosus (Mendonça et al., 2011). The outflow sediment plume of the São Francisco river might act as a BGF for some organisms. In addition, the turbidity and low salinity caused by freshwater discharge inhibits the development of coral reefs at Sergipe and Alagoas, which could also act as another BGF to a range of benthic reef species. The absence of reefs allows the tide to penetrate local estuaries, contributing to the establishment of mangroves, changing the coastal ecosystem (da Silva et al., 2016) and creating potential BGF. Therefore, the combination of these three factors might be acting differently in different species and places within Region II.
Between latitudes 16° and 20.5° S, the continental shelf becomes shallower and wider to form the Abrolhos Archipelago Basin and eastward Vitória-Trindade seamount chain. This region splits the Brazilian coastline into two sections, especially during past periods Quaternary’s glacial maxima, when the sea level was 110 m lower than the present day (R. Peterson & Stramma, 1991; Stramma & England, 1999). The emersion of wider offshore reefs and islands areas in the Abrolhos Arquipelago and the tops of Vitoria-Trindade seamount chain caused strong changes in the flow of the Southern Brazil Current, restricting gene flow along the Brazilian coastline. In addition, during glaciations, the Subtropical Convergence could also act as a barrier, when occurring near Vitória-Trindade seamount chain (20.5° S) (R. Peterson & Stramma, 1991; Stramma & England, 1999), which is currently located in southern Brazil and Uruguay (R. Peterson & Stramma, 1991). The interaction between the Abrolhos Basin, The Vitoria-Trindade seamount and the changes in oceanic connectivity during glacial maxima have been suggested as major extant barriers of gene flow for several organisms, such as mollusks (Crassostrea spp.: Lazoski et al., 2011), crustaceans (Excirolana braziliensis : Hurtado et al., 2016) and polychaete (Perinereis spp.: Paiva et al., 2019). The genetic discontinuities between populations sampled north and south of the Abrolhos Basin and the Vitória-Trindade seamount region most likely originated in the Pleistocene and remained structured to this day, even after the barrier is no longer active.
Region III (20.5° – 27° S latitude) ranges from the Vitória-Trindade seamount chain to Santa Catarina representing a region with the lowest levels of BGF occurrence. Populations in this area tend to retain new mutations and low genetic diversity, which is a signature of sudden population expansion (Grant & Bowen, 1998). Several studies reports this particular genetic pattern in the region such as fish species (da Silva et al., 2016; Machado et al., 2017; Santos et al., 2006), macroalgae species (Crassiphycus caudatus: Ayres-Ostrock et al., 2019; Hypnea pseudomusciformis : Nauer et al., 2019), marine vascular plants (Rhizophora spp.: Francisco et al., 2018), a cnidarian (Mussismilia hispida : Peluso et al., 2018), nemerteans (Ototyphlonemertes spp.: Andrade, Norenburg, & Solferini, 2011), polychaetes (Perinereis spp.:Paiva et al., 2019), and a sea turtle (Caretta caretta : Reis et al., 2010). Sympatric tropical marine species undergoing sudden population expansion reflects a shared past history of generalized low effective population sizes caused by bottlenecks or founder events. This concordance is most likely the result of demographic expansion of tropical populations within Region III promoted by the gradual warming since the last glacial maxima. This region is, therefore, an area of relative smaller number of BGF and higher panmixia. We found only three studies with opposite results to this pattern: two fish studies (Galeocerdo cuvier : Carmo et al., 2019; Macrodon atricauda : Rodrigues et al., 2014), and a dolphin study (Pontoporia blainvillei : Secchi et al., 1998). These three species also share the fact that higher genetic diversity was detected in populations located south of the Vitoria-Trindade seamount chain compared to populations sampled north of this region and their geographic distribution extends into the temperate zone, towards Uruguay and northern Argentina. Hence, they are not exclusively tropical species.
The Cabo Frio seasonal upwelling system in the north of the Rio de Janeiro (around 22° S) (Valentin, Andre, & Jacob, 1987) has been considered a popular BGF hypothesis for coastal benthic marine species (Peluso et al., 2018). The upwelling occurs with great intensity during austral summer. It is a consequence of seasonal northeast winds, abrupt change in the continental shelf shape and slope, resulting in the upwelling of the South Atlantic Central Water (Valentin et al., 1987). The Cabo Frio upwelling system could act as a barrier to gene flow in two ways: a) physical/physiological barriers due to conspicuous shifts in sea temperatures, or b) local selection limiting recruitment of certain genotypes (Peluso et al., 2018). We detected the presence of a weak sign of phylogeographic concordance in this region, however only a few studies support the existence of a BGF in this area. Studies that identified the Cabo Frio upwelling system as a BGF include a fish species (Atherinella brasiliensis : Cortinhas et al., 2016), crustaceans (Excirolana braziliensis : Hurtado et al., 2016;Litopenaeus schmitti : Maggioni, Rogers, & Maclean, 2003), and a cetacean (Tursiops truncatus : de Oliveira et al., 2019). The upwelling system might be acting more as a genetic filter rather than a barrier to the majority of marine organisms (Peluso et al., 2018).
The lowest values of BGF frequency observed in Region III coincides with poorly studies areas between southern São Paulo state and northern Santa Catarina State. This is a poorly sampled region due to the lack of urbanization in the area. It is also characterized by sandy beaches, smaller and shallow rocky shores, and two large estuaries, the Paranaguá bay and the Guaratuba estuary. Interestingly, the two lowest BGF frequency values observed in this study matched precisely these two estuaries, 6.94% and 7.25%, respectively. Large estuaries are expected to act as BGF because they often disrupts coastal marine environmental conditions by dumping large quantities of freshwater, nutrients, sediments, influencing tides and coastal currents. Instead, our results suggest that these two estuaries promote genetic connectivity among costal marine populations.
Low levels of BGF frequency in Region III is interrupted at south Santa Catarina state and northern Rio Grande do Sul frontier and highlights the beginning of phylogeographic Region IV. Region IV has several consecutive estuaries intercalated with open sea areas, which could be acting as BGF, specially to fish species (Beheregaray & Levy, 2000; Rodrigues et al., 2014), cetaceans (Costa et al., 2015; Fruet et al., 2014; Secchi et al., 1998), and crustaceans (Weber & Levy, 2000). Geographically close estuaries could be very different from each other, in salinity, temperature, water quality and food stocks. Thus, populations can use different estuaries for either reproduction or foraging. Therefore, geographically close populations using different estuaries could present genetic discontinuity due to differences in estuaries usage (Weber & Levy, 2000). In addition, the observed differentiation could be related to the subtropical confluence of the warm saline, Brazil Current, and the cold, northerly Malvinas’ current (R. Peterson & Stramma, 1991). The northern limit of this confluence moves seasonally from 30 – 35° S during the winter to 40° S – 46° S during the summer (R. Peterson & Stramma, 1991). This oceanographic processes has been proposed a BGF (Cortinhas et al., 2016; Vasconcellos, Lima, Bonhomme, Vianna, & Solé-Cava, 2015). Lastly, this region also coincides with the north end of the Rio Grande do Sul state, a region that include the world’s longest beach, Cassino beach, with 220 kilometers of unconsolidated sandy substratum. Long stretches of sandy beaches have been considered putative BGF for hard bottom marine species (Nauer et al., 2019; Trovant et al., 2016). However, we could not test if Cassino beach can be considered a BGF because this region is located at the geographic extreme of our study area. This region encompasses the Cape Santa Marta which might act (or might have acted) as a BGF by deflecting the Malvina’s Current offshore (R. Peterson & Stramma, 1991). Capes are often regarded as BGF, e.g. Cape Canaveral (Gurgel et al., 2004; Reeb & Avise, 1990), by deflecting coastal boundary current offshore.
The SEC split and Vitória-Trindade seamount chain represent more noticeable BGF for fishes than any other taxa. An intermediate BGF at northern Rio Grande do Sul state also occurs. For crustacean data, the SEC split is not a major BGF, as observed for other taxa. The main crustacean BGF occurs at the northern Rio Grande do Sul state. For mollusks data, only the SEC split seems to be the main BGF concordance, acting as a barrier to almost 50% of the studied mollusk taxa, followed by plateau from São Francisco river mouth and the region of lowest BGF registered in this study, within Region III. For the cnidarian data, there is a strong BGF at northernmost sampled zone and two secondary peaks: one at Abrolhos (southern Bahia state) and another in Santos city (São Paulo). However, the cnidarians data should be interpreted with care, considering the low number of studies (n > 5).