Introduction
Comparative phylogeography is a powerful tool that looks into multiple
independent studies to describe broad-scale concordant patterns of
population genetic structure across space, taxa and molecular markers
(Bowen et al., 2014). Comparative phylogeography also attempts to
identify the processes responsible for the development and maintenance
of such concordant patterns. The presence of concordant phylogeographic
patterns, or spatially congruent phylogeographic breaks among species,
often represents shared evolutionary histories across phylogenetically
distinct taxa, and hence, identify historical, climatic, geological or
ecological forces capable of shaping the evolution of entire biotas
(Arbogast & Kenagy, 2001; Avise, 2000; Dawson, 2013; Hickerson et al.,
2010). The search for phylogeographic concordance has become a central
objective in comparative phylogeography (Avise, 2000) and results from
comparative phylogeographic analyses have major impacts on environment
conservation programs worldwide (Olson et al., 2001; Spalding et al.,
2007). The presence of a phylogeographic break means that a previous
genetically continuous population can now be identified as two, or more,
genetically distinct populations. Population genetic differentiation is
an essential step towards speciation and can only occur in the absence
of gene flow. Historical and vicariance events that interrupt gene flow
are termed barriers to gene flow (BGF). Consequently, BGF are
intrinsically associated to the formation and maintenance of
phylogeographic breaks. Wherever a phylogeographic break occurs, most
likely one or more extinct or extant BGF also occurs.
BGF in the marine environment are not easily detected due to the
stronger connectivity promoted by water-mediated dispersal and the
existence in several organisms with larval phases with high dispersal
capabilities (Imron, Jeffrey, Hale, Degnan, & Degnan, 2007).
Topographic features such as bluffs, capes, promontories, and
peninsulas, together with ocean currents, long stretches of sandy
beaches, and the mouth of major rivers have been identified as BGF in
coastal marine environments (Bilton, Paula, & Bishop, 2002; Defeo,
1996; Defeo & De Alava, 1995; Wares, Gaines, & Cunningham, 2001).
Pleistocene glaciations also represent climatic processes that have
played major roles redefining BGF in the marine environment and shaping
recent marine biological evolution worldwide. However, glaciation
effects on marine biota are better comprehended in the northern
hemisphere where its influence was more severe (Guralnick, 2006;
Pfenninger, Posada, & Magnin, 2003; Trewick et al., 2002). In tropical
marine habitats, which are areas less influenced by past glaciations,
only a few barriers are apparent and most putative BGF remain poorly
studied (Rocha, Craig, & Bowen, 2007).
To date, comparative phylogeography studies and phylogeographic
literature reviews include those performed for the USA terrestrial and
marine biotas (Shafer, Cullingham, Côté, & Coltman, 2010; Soltis,
Morris, McLachlan, Manos, & Soltis, 2006), the South American
terrestrial biota (Turchetto-Zolet, Pinheiro, Salgueiro, & Palma-Silva,
2013), south Europe terrestrial biota (Feliner, 2011; Taberlet,
Fumagalli, Wust-Saucy, & Cosson, 1998), Australian terrestrial and
marine biota (Byrne, 2008; Teske, Sandoval-Castillo, Waters, &
Beheregaray, 2017), and African ungulates (Lorenzen, Heller, &
Siegismund, 2012) and those that targeted a specific group of organisms
(e.g. Satler & Carstens, 2016). No comparative phylogeography analyses
or phylogeographic literature reviews have yet focused the Brazilian
marine biota. Brazil possesses one of the longest north-south tropical
coastlines in the world, with approximately 7,000 km, spanning 37
degrees of latitude (from 4° North to 33° South).
The first studies on Brazilian marine phylogeography started in early
90’s (Aron & Solé-Cava, 1991; Russo & Solé-Cava, 1991) based on
allozymes, an extensively used technique in population genetic studies
in the previous decades. Aron & Solé-Cava (1991) did not identify
genetic structure in Botryllus niger (an ascidian) populations
collected between Espírito Santo and Rio de Janeiro, where Russo &
Solé-Cava (1991) could not detect genetic structure in Bunodosoma
caissarum (an anemone) within Rio de Janeiro State. Since then, a large
number of articles using different markers, targeting different spatial
scales, applying different sampling designs and looking at wide range of
phylogenetically distant taxa have been published.
Several putative BGF have been proposed in the literature to explain
genetic discontinuities along the Brazilian coast. Chiefly among them,
we have: (a) the mouth of major rivers such as the Amazon, São
Francisco, Paraguaçu, Jequitinhonha, Doce, and Paraíba do Sul (da Silva,
Marceniuk, Sales, & Araripe, 2016; Machado et al., 2017); (b) the split
of the South Equatorial Current (SEC) in two opposing boundary currents,
giving rise to the southward Brazil Current and the northward North
Brazil Current (Bezerra et al., 2018; Cortinhas et al., 2016); (c) the
Cabo Frio coastal upwelling system (Cortinhas et al., 2016; Hurtado et
al., 2016) and; (d) the Cassino beach, the longest stretch of sandy
beach in the world located in southern Brazil between latitudes 29° S
and 32° S (Nauer, Gurgel, Ayres-Ostrock, Plastino, & Oliveira, 2019;
Trovant et al., 2016). In several phylogeographic studies, genetic
discontinuities coincide with these coastal features, allowing
researches to identify them as potential BGF (e.g. Hurtado et al., 2016;
Lazoski, Gusmão, Boudry, & Solé-Cava, 2011; Paiva, Mutaquilha,
Coutinho, & Santos, 2019), but sometimes phylogeographic structure does
not match such features (e.g. Carmo et al., 2019; Rodrigues et al.,
2014; Secchi, Wang, Murray, Rocha-Campos, & White, 1998). Extinct BGF
could have produced genetic discontinuities that perpetuate over time
and can be observed in today’s populations, even in the absence of
extant BGF. One probable example of such case is the Vitoria-Trindade
seamount chain, which geographically includes the Abrolhos Reef system.
During Quaternary’s glacial maxima, the drop in sea level emerged large
eastward inflected areas of the Brazilian continental shelf, including
seamounts, splitting the continent’s coastline into two sections: (a) a
warmer, possibly subtropical, northern bioregion influenced by a weaker
Brazil Current; and (b) a colder, probably temperate, southern bioregion
influenced by a stronger Malvina’s Current (Fig. 1). This BGF has been
proposed to explain genetic discontinuities of several marine taxa such
as mollusks (Crassostrea spp.: Lazoski et al., 2011), crustaceans
(Excirolana braziliensis : Hurtado et al., 2016), polychaetes
(Perinereis spp.: Paiva et al., 2019), and red macroalgae
(Crassiphycus caudatus : Ayres-Ostrock et al., 2019; Hypnea
pseudomusciformis : Nauer et al., 2019).
In the last three decades of cumulative publications on the population
genetics and phylogeography of Brazilian’s marine species, no literature
review or comparative phylogeographic study have been made.
Consequently, we still do not know which BGFs, whether one of those
listed above or others yet to be revealed, imprinted the largest effect
on Brazil’s marine biota. Therefore, the objectives of this study were:
(a) to provide a comprehensive literature synthesis of Brazil’s marine
phylogeography; and (b) to perform a comparative phylogeography analysis
to identify major BGF along the Brazilian coastline. Comparative
phylogeography has traditionally being executed by matching concordant
patterns, without explicit quantitative measurements of the degree of
concordance (or discordance). This limitation reduces the ability of the
discipline to produce predictive models capable to identify new areas of
major BGF concordance. This study also provides the first quantitative
measure of phylogeographic concordance in the marine environment that
allowed us to model and predict the degree to which BGF along the
Brazilian coast are responsible for genetic structuring and speciation
across multiple taxa.