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).