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.