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\begin{document}

\title{Barriers to gene flow along the Brazilian coast: a synthesis and data
analysis}



\author[1]{Nuno Martins}%
\author[2]{Leonardo Macagnan}%
\author[3]{Valéria Cassano}%
\author[4]{CARLOS GURGEL}%
\affil[1]{USP}%
\affil[2]{Federal University of Santa Catarina}%
\affil[3]{Universidade de São Paulo}%
\affil[4]{Universidade Federal de Santa Catarina}%


\vspace{-1em}



  
  \date{June 02, 2024}


\begingroup
\let\center\flushleft
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\selectlanguage{english}
\begin{abstract}
Barriers to gene flow (BGF) play a pivotal role in the dynamics of
population genetics promoting genetic differentiation, thus, are
inexorably associated with the development and maintenance of
phylogeographic structure. Phylogeographic structure resulting from BGF
represents data that help the management of natural genetic resources,
aiding in the recognition of areas of conservation interest. Several
geographic and oceanographic processes found along the Brazilian coast
have been proposed as BGF. However, no consensus exist identifying which
of them represents the most important in shaping biodiversity.
Therefore, this study provides a synthesis of the scientific literature
on Brazilian marine phylogeography and used published data to build
datasets that allowed us apply linear (lm) and generalized additive
models (gam) to identify spatially congruent phylogeographic breaks
among marine species (as areas of high BGF frequency occurrence). Lm
identified a significant negative correlation between the occurrence of
BGF and latitude, suggesting that population in the tropics are
genetically more structured than in higher latitudes. This result bears
strong association with the latitude species diversity gradient observed
worldwide. Gam identified Cape S\selectlanguage{ngerman}ão Roque (05° 28' S) as the main BGF for
populations with continuous distribution along the Brazilian coast. Cape
São Roque is located near the center point region where the South
Equatorial Current splits into the northward North Brazil Current and
the southward Brazil Current. This study represents the first literature
synthesis of Brazil's marine phylogeography and provides a novel
explicit quantitative approach to comparative phylogeography.%
\end{abstract}\selectlanguage{ngerman}%



\sloppy


\textbf{Barriers to gene flow along the Brazilian coast: a synthesis and
data analysis}

Nuno T. Martins\textsuperscript{1,3,*}, Leonardo B.
Macagnan\textsuperscript{2}, Val\selectlanguage{ngerman}éria Cassano\textsuperscript{1}, Carlos
Frederico D. Gurgel\textsuperscript{2}

\textsuperscript{1}Universidade de São Paulo, Instituto de Biociências,
Departamento de Botânica, São Paulo, SP 05508-090, Brazil

\textsuperscript{2}Universidade Federal de Santa Catarina, Centro de
Ciências Biológicas, Departamento de Botânica, Florianópolis, SC
88040-900, Brazil

\textsuperscript{3}ORCID: https://orcid.org/0000-0003-1912-0443

\textsuperscript{*}Corresponding author: nunotmartins@usp.br

\textbf{Running title} : Brazilian marine phylogeography



\textbf{Abstract}

Barriers to gene flow (BGF) play a pivotal role in the dynamics of
population genetics promoting genetic differentiation, thus, are
inexorably associated with the development and maintenance of
phylogeographic structure. Phylogeographic structure resulting from BGF
represents data that help the management of natural genetic resources,
aiding in the recognition of areas of conservation interest. Several
geographic and oceanographic processes found along the Brazilian coast
have been proposed as BGF. However, no consensus exist identifying which
of them represents the most important in shaping biodiversity.
Therefore, this study provides a synthesis of the scientific literature
on Brazilian marine phylogeography and used published data to build
datasets that allowed us apply linear (\emph{lm} ) and generalized
additive models (\emph{gam} ) to identify spatially congruent
phylogeographic breaks among marine species (as areas of high BGF
frequency occurrence). \emph{Lm} identified a significant negative
correlation between the occurrence of BGF and latitude, suggesting that
population in the tropics are genetically more structured than in higher
latitudes. This result bears strong association with the latitude
species diversity gradient observed worldwide. \emph{Gam} identified
Cape São Roque (05° 28' S) as the main BGF for populations with
continuous distribution along the Brazilian coast. Cape São Roque is
located near the center point region where the South Equatorial Current
splits into the northward North Brazil Current and the southward Brazil
Current. This study represents the first literature synthesis of
Brazil's marine phylogeography and provides a novel explicit
quantitative approach to comparative phylogeography.

\textbf{Keywords}

Brazil, genetic breaks, gene flow, geographic barriers, marine,
phylogeography

\textbf{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 \emph{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 \emph{Botryllus niger} (an ascidian) populations
collected between Espírito Santo and Rio de Janeiro, where Russo \&
Solé-Cava (1991) could not detect genetic structure in \emph{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 (\emph{Crassostrea} spp.: Lazoski et al., 2011), crustaceans
(\emph{Excirolana braziliensis} : Hurtado et al., 2016), polychaetes
(\emph{Perinereis} spp.: Paiva et al., 2019), and red macroalgae
(\emph{Crassiphycus caudatus} : Ayres-Ostrock et al., 2019; \emph{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.

\textbf{Materials and methods}

Literature survey

The database used for this synthesis was compiled from searches in the
Web of Science\textsuperscript{®} (Institute of Scientific Information,
Thomson Scientific). Web of Science is an online academic database from
ISI Web of Knowledge\textsuperscript{®} that provides access to
information about indexed research journals worldwide. We searched all
Web of Science databases for scientific articles published from 1987
(regarded as the birth of phylogeography; Avise, 1987) to 2019 using the
following keywords and Boolean command combinations: population*
genetic* OR phylogeo*; AND Brazil*; AND ocean* OR sea* OR island OR reef
OR rocky shore OR benthic OR marine OR coast*. Preliminary results
identified 1380 articles, several of them outside the target parameters.
Thus, we used the following secondary filters to further sort
phylogeographic articles addressing specifically marine species that
occur in Brazil: NOT ``Atlantic forest'' OR rainforest* OR freshwater.
After applying secondary filters, 1170 articles remained.

A third-level filtering was performed by hand, visually scanning each
article (i.e. title, abstract, hypotheses, material and methods, or
results), and excluding those with the following characteristics: review
articles; conference abstracts; technique articles; articles that
studied viruses and bacteria (marine or otherwise) and human diseases;
articles that presented only one sampled population in Brazil; articles
that were purely taxonomic; articles that involved only populations
located in offshore oceanic islands (i.e. São Pedro - São Paulo
Archipelago, Trindade seamount chain Island, Rocas Atoll, Fernando de
Noronha Archipelago, and Rio Grande seamount); articles that involved
non-native Brazilian marine species; articles that despite claiming they
implemented phylogeographic analyses, did not use molecular data to test
for the presence of phylogeographic structure among populations; and
articles addressing taxa that live in close proximity to the marine
environment but do not depend in any way of the marine ecosystems to
exist. Thus, this study focused on empirical, molecular data-driven
phylogeographic articles that minimally addressed the Brazilian's
continental coastline and native marine biota, including marine birds
and plant mangrove species.

All selected articles were fully read. A database was built based on
information extracted from the articles and included: year of
publication; species taxonomy assigned to 16 categories (Ascidiacea,
Aves, Cetacea, Cnidaria, Crustacea, Echinodermata, Fishes, Kinorhynch,
Mollusca, Nemertea, Otariidae, Plantae, Platyhelminthes, Polychaeta,
Porifera, and Testudinata); number of analyzed taxa per article; sample
site locations (city, state and geopolitical zone name, coordinates);
genetic markers used (technique, genome and name of used genes);
presence or absence and number of genetic discontinuities reported,
locations from where genetic discontinuities were reported;
classifications of species habitat (as benthic, pelagic, or aerial) and
functional forms (invertebrates, vertebrates, or plants). Basic
statistics were calculated from this database using Microsoft Excel
tools.

In this study we refer to \emph{article} (\emph{s} ) each and every
publication or unique reference, and we refer to '\emph{study}
(-\emph{ies} )' each species with phylogeographic information found
within each article. Therefore, some articles were comprised of only one
study, while multi-taxon articles contained two or more studies (taxa).

Dataset preparation

A data matrix comprised by all sample sites reported in
all\emph{studies} was built from the database described above. For each
study captured in our database, sites where sampled populations occurred
were logged in the data matrix as 0's. Sites located between sampled
populations where genetic discontinuities were recorded, and hence
putative BGF existed, were logged as 1's. Thus, for each study, whenever
panmixia were detected, geographic ranges between genetically
homogeneous populations were marked as a string of zeros between sample
sites. From this data matrix, we built a frequency data matrix by
summing all putative BGF occurrences across logged studies, normalized
by the total number of studies that included each site (Table S1).

A large normalized BGF frequency value in a given site indicates that a
large number of studies identified that particular site as either a BGF
or a location of high probability of occurrence of BGF. Consequently,
those sites can be considered locations of high BGF concordance.
Conversely, a small value means either absence of BGF in a particular
site (= area of high genetic connectivity) or that a small number of
articles and studies included those sites within the range of their
sampling designs. A distribution of the frequencies of occurrence of
putative BGF along a latitudinal gradient (which is the case for most of
the Brazilian coast) can be easily applied to comparative
phylogeography, because this distribution represents the likelihood for
which a phylogeographic break exists in a given location given by
multiple empirical studies. Thus, the frequency of occurrence of
putative BGF not only quantifies but also describes how one of the most
important concepts in comparative phylogeography is distributed in
space: concordance in the spatial distribution of phylogenetic breaks
across co-occurring species (type III concordance in Avise, 2000).

Modelling

For modeling analyses, we used the normalized BGF frequency dataset
described above. Due to the smaller number of studies and hence larger
numbers of missing data from sampling sites at Brazil's northernmost and
southernmost locations, those sites were excluded from the analysis. The
resulting spatial range included in the models varied between central
Pará (Belém: 01° 24' S 48° 29' W) and south of Rio Grande do Sul (Patos
lagoon inlet: 31° 22' S). This encompassed 201 of the 211 sites included
in the original dataset. A general linear model (\emph{lm} ) was
initially used to test for the presence of significant non-random
differences in the frequency distribution of BGF concordances across
latitudes along the Brazilian coast. We used the \emph{glm} function
available in the package \emph{stats} implemented in R (R Core Team,
2020) with the default parameters. Initial data exploration showed that
the response of frequency distribution of BGF concordances to latitude
was non-linear. Then, generalized additive modelling (\emph{gam} ) was
used with latitude as a smooth effect. First, we modelled all data
combined and then individually each taxa with the greatest number of
available data (fishes, crustaceans, mollusks and cnidarians). We used
the \emph{gam} subroutine available in the \emph{mgcv} package (Wood,
2017) implemented in R. We fitted the \emph{gam} 's using Gaussian
distributions including for logistic regression. We also used a smooth
term with a cubic regression or cyclic cubic regression spline (for
fishes and crustacean data) to represent latitudinal variation.
Several\emph{gam} models were tested varying the smooth terms
parameters:\emph{fx} (fix the degrees of freedom on a regression spline
model), the\emph{K} (dimension of the basis used to represent the smooth
term) and the \emph{bs} (smoothing term) parameters. The optimal model
was selected using the \emph{gam.check} tool (Wood, 2017). Model
validation was assessed using the generalized cross-validation (GCV)
index, the Unbiased Risk Estimation (UBRE), the ''\emph{starry-sky} ''
patterns in the residuals versus linear prediction graph, and a the
linear relationship between response parameter and the fitted graph. The
Effective Degree of Freedom (EDF) was used to test if \emph{gam} was a
valid method to analyze our datasets (i.e. EDF \textgreater{} 2). Model
quality was also assessed by comparing adjusted R\textsuperscript{2} and
the explained deviance.

Differences between average values of BGF frequencies among
phylogeographyc regions identified in the \emph{gam} results were using
analysis of variance (ANOVA) with type-3 sum of squares. Normality and
homogeneity assumptions of variances were tested using Shapiro-Wilk and
modified robust Brown-Forsythe Levene-type test, respectively (Zar,
1999). Tuckey was used as the post hoc test. Analyses were done in R (R
Core Team, 2020) using \emph{aov} function in \emph{car} package, and
adopting an alpha of 0.05.

\textbf{Results}

Literature survey

The final number of articles was 159, representing 195 studies, covering
211 sites. The northern and southernmost sampling locations were
Oiapoque (latitude: 4° N) and Chuí (latitude: 34° S), respectively,
spreading across \textasciitilde{}7,000 km, representing nearly the
entire Brazilian coast. Articles comprised of only one study represented
80\% of the total, followed by articles composed by two (11\%), three
(6\%), and four (2\%) studies. Only one article presented 6 studies of
which only 3 were used based on the second-level filtering criteria
listed above (Nunes, Norris, \& Knowlton, 2011). The oldest articles
were published in 1991 (two articles) and the newest in 2019 (12
articles). Since 1991 the number of publications per year increased,
particularly after the year 2001 (four articles/year) when a steady
increase is noticed, culminating in the publication of at least 10
articles per year after 2014 (Fig. 2). The five journals with the
highest number of articles were listed in Table 1.

Markers

Ten different molecular techniques were reported in the literarure:
allozymes, DNA sequencing, ddRAD, RAPD, ISSR, AFLP and RFLP, cariology,
SNP and microsatellites (Fig. 3A). DNA sequences obtained via automated
Sanger sequencing were the most commonly used type of molecular data
(71\% studies). Among DNA sequence markers, a total of 38 different
genes were used; 16, 19 and 3 encoded in the mitochondrial, nuclear and
chloroplast genomes, respectively. DNA sequencing of mitochondrial genes
was by far the most used technique among all markers and across all
studies (80\%), followed by the DNA sequencing of nuclear (18\%) and
chloroplast-encoded markers (2\%). Within the mitochondrial genome, the
D-loop region and the COI DNA barcode marker were the most used marker
(34\% each), followed by the cytochrome B gene (15\%). The number of
articles using microsatellites or allozymes were similar (12\% and 10\%,
respectively). The first allozyme study was published in 1991 (Aron \&
Solé-Cava, 1991; Russo \& Solé-Cava, 1991) and the last in 2018 (Pazoto,
Ventura, Duarte, \& Silva, 2018). Only four articles (6\%) targeted
autotrophic organisms, two terrestrial vascular plants (mangroves) and
two red macroalgae, and two of them used chloroplast-encoded markers
(Ayres-Ostrock et al., 2019; Mori, Zucchi, Sampaio, \& Souza, 2015).
Only one more recent article used the SNP technique (Siccha-Ramirez et
al., 2018).

Geographic coverage, taxonomic coverage, habitats diversity \&
functional forms

Brazil has 17 geopolitical states along its coastline and they were all
included in this synthesis (Table 2). The geopolitical state with the
largest number of articles reporting at least one sample site inside its
borders was the Rio de Janeiro (48\%, 93 studies), followed by São Paulo
(46\%, 89 studies) and Bahia (44\%, 86 studies). The least sampled
states were Piauí (4\%, eight studies), Sergipe and Amapá (6\%, 12
studies). Only 16 high-ranked taxonomic groups were identified in all
articles (Fig. 3B). The state with the largest number of studied taxa
was São Paulo with 14 taxa followed by Rio de Janeiro (13 taxa) and
Santa Catarina (12 taxa). The states with the smallest number of sampled
taxa were Amapá and Alagoas with only 4 taxa each (Table 2).

Three taxa presented sample sites located within only one state: otaries
(Rio Grande do Sul: Artico et al., 2010), echinoderms (Rio de Janeiro:
Calderón, Ventura, Turon, \& Lessios, 2010; Duarte, Ventura, \& Silva,
2016; Pazoto et al., 2018; Wangensteen, Turon, Pérez-Portela, \&
Palacín, 2012), and Kinorhynchs (São Paulo: Randsø, Domenico, Herranz,
Lorenzen, \& Sørensen, 2018). Together with flatworms (=
Platyhelminthes, Marigo et al., 2015), phylogeographic studies targeting
these taxa concentrated their sampling in the southern Brazil
(\textgreater{} 21° S). Fishes and mollusks presented the most
comprehensive and spatially widespread sampling across Brazil (100\%
states), followed by crustacean (16/17 states), and plants (14/17
states). Fishes were the most studied taxon encompassing 32\% of all
studies, followed by crustaceans (21\%) and mollusks (10\%) (Fig. 3B).
Of all studied taxa, 49\% were invertebrates, followed by 47\% of
vertebrates, and 4\% plants, including algae (Fig. 3C). Regarding
habitat, 63\% studies targeted benthic species, 34\% pelagic, and 3\%
aerial (i.e. coastal and marine birds) (Fig. 3D).

Models

The site with the highest value of BGF concordance was Galinhos (05°03'
S, 36°45' W); north of Rio Grande do Norte State (27 \%). The linear
model identified a statistically significant negative relationship
between frequency in the occurrence of phylogenetic breaks (BGF) and
latitude, R\textsuperscript{2} = 0.4, p \textless{} 0.001 (Fig.
4).\emph{Gam} results from all data combined (= total analysis)
identified four geographic regions with distinct patterns of BGF
frequency distribution along the Brazilian coast, herein dubbed
phylogeographic Regions I-IV (Fig. 5). Anova detected significant
differences in the average amount of BGF frequencies among these
regions. Pairwise tests found no differences between Regions I and II
but Regions III and IV where different from all the others (Fig. 6).
\emph{Gam} Region I (0° S -- 10° S) was located in northern Brazil and
presented a bell-shaped BGF frequency distribution with the greatest
modelled values of BGF concordance in the entire Brazilian coast.
\emph{Gam} identified Natal city in central Rio Grande do Norte (05° 46'
S) as the region with the highest value of BGF concordance (Fig. 5).
Region II showed a relative homogenous distribution of BGF concordances
south of 10° S until the Vitória-Trindade seamount chain region at 20.5°
S. Region III (20.5° S - 27° S) exhibited an inverted bell-shaped
distribution with the lowest BGF concordance values, ranging from
central Espírito Santo to northern Santa Catarina (Itajaí: 26° 54' S).
Region IV was characterized by a moderate bell-shaped distribution of
BGF concordance values that started at northern Santa Catarina and
extended to the north-end of longest uninterrupted sandy seashore in the
world (Patos lagoon inlet: 31° 22' S). In Region IV the \emph{gam}
maximum BGF concordance value occurs in southern Santa Catarina, Cape
Santa Marta, 28° 36' S (Fig. 5).

\emph{Gam} for the four most studied taxa (fishes, crustaceans,
mollusks, and cnidarians) produced patterns of BGF frequency
distribution similar to those reported in the total analysis, although
slightly differences were noted (Figs. 7A-D). Fishes, the most data-rich
taxon (Fig. 7A), presented the I-IV region pattern reported in the total
analysis but the main peak of maxima was observed at the southern-end of
Region II, around central Rio de Janeiro (Saquarema: 22° 56 S, 42° 29
W), followed by a slightly lower maxima in Region I. Latitudes or a
string of adjacent sites with values of BGF frequency distribution equal
to 0\% identifies regions of widespread panmixia, and that was the case
for fish populations sampled between Paraná (Laranjeiras Bay: 25° 24' S)
and northern Santa Catarina (Itajaí: 26° 54' S). A thirst albeit small
maxima was also observed inside Region II, coinciding with central Bahia
state (Barra Grande: 13° 52' S). Accordingly, fishes'
\emph{gam}presented four regions of BGF frequency maxima: northern Rio
Grande do Norte (around Galinhos: 05° 03' S, 36° 45' W), central Bahia
(around Barra Grande: 13° 52' S), central Rio de Janeiro (around
Saquarema: 22° 56 S, 42° 29 W), and southern Rio Grande do Sul (near
Patos lagoon inlet: 31° 22' S) (Fig. 7A).

Even though the crustacean \emph{gam} presented similar topology to
those obtained from the other three taxa and the total
evidence\emph{gam} , this taxon showed slightly unique pattern of BGF
frequency distribution (Fig. 7B). The greatest modelled BGF frequency
value for crustaceans along the Brazilian coast occurred near Cape Santa
Marta, 28° 36' S (23\%), in phylogeographic Region IV. The north and
northeastern Brazilian coast showed a somewhat homogenous BGF frequency
distribution ranging from Pará (Belém: 01° 24' S), to south Espírito
Santo (Guarapari: 20° 40' S) (Fig. 7B). An increase in the values of
crustacean BGF frequency, denoting a bell-shape topology, was observed
in southeastern Brazil, starting in Guarapari (Espírito Santo), peaking
at central Rio de Janeiro (within the Cabo Frio district, 22° 57' S) and
ending in northern São Paulo (Ubatuba: 23° 26' S) (Fig. 7B). A long
region of lower BGF frequencies (similar total dataset Region III)
occurred south of Ubatuba (São Paulo) and extended to north Santa
Catarina (Itajaí: 26° 54' S).

For mollusks and cnidarians, recorded BGF values in the literature are
absent west of Belém (01° 27' S, 48° 29' W) and Fortaleza (03° 43' S,
38° 31' W), respectively, and south of Florianópolis (27° 36' S) for
both groups (Figs. 7C and 7D). \emph{Gam} results for mollusks and
cnidarians presented several similarities. Mollusks and cnidarians
showed the greatest values of BGF frequency distribution in their
northernmost latitudes within Brazil (phylogeography Region I in the
total evidence \emph{gam} ), with maximum values reaching 50\% and 75\%,
respectively. For mollusks, the maximum BGF concordance occurred around
west of Fortaleza at Ceará state, all the way to Maranhão state (Fig.
7C). For cnidarians, the region of maximum BGF frequency values occurred
north of João Pessoa, Paraíba (Fig. 7D). Mollusks presented an average
of 21\% of BGF concordances spread across a large portion of the
Brazilian coast, from latitude 04° 50' S to 25° 24' S, corresponding to
Region II in the total dataset results (Fig. 5). Cnidarians also
presented a Region II-like distribution between latitudes 10° S and 20°
S. Interestingly, results from all four taxa showed a region of
BGF\emph{gam} minima (Figs. 5A-D) that tends to coincided with the
minima observed in the total evidence \emph{gam} between latitudes 20° S
and 25° S (= Region III in Fig. 5). This region of BGF frequency minima
was always followed by an increase in BGF frequency farther south
(Region IV), passing 25° S latitude and generally peaking at Cape Santa
Marta (28° 36' S).

\textbf{Discussion}

Literature synthesis

Phylogeography was conceived as a science in 1987, since then the number
of publications has grown exponentially. In Brazil, the first two marine
phylogeographic studies were both published in 1991 using allozymes
(Aron \& Solé-Cava, 1991; Russo \& Solé-Cava, 1991). New publications
have increased ever since. The years 2016 and 2018 presented the highest
number of Brazilian marine phylogeographic publications to date (15
articles). Considering the 16 taxonomic groups assessed in this study,
fishes have been the most studied taxon, accounting for 33\% of all
publications. This is more than the second and third most studied taxa
combined (crustaceans 21\%, mollusks 9\%). A conspicuous publication
bias towards fish phylogeographic studies is observed in the literature
globally. Beheregaray (2008) reviewed all phylogeographic articles
published between 1987 and 2006 and fishes were ranked second, after
mammals, as the taxonomic group with the largest number of publications
without much difference whether they were freshwater (45\%) or marine
species (55\%). Turchetto-Zolet et al. (2013) reviewed all
phylogeographic articles published on South America terrestrial and
freshwater biota between 1987-2011 and reported fishes as the second
ranked taxonomic group (13\%) together with overall invertebrates and
second only to plants (17\%). This bias towards fishes is probably due
to their economic importance as human food and ecotourism, relative
easier taxonomic identification, simple life-cycle and ploidy, the
availability of well-suited genetic markers, and probably, the existence
of a large number of hired expertise in research institutions.
Differently, otaries, Kinorhynchs and flatworms presented very localized
sampling due to low number of publications (one each).

The numbers of marine vertebrate and invertebrate studies in Brazil were
quite even, 47\% and 49\%, respectively. This is opposite to what was
recorded by Beheregaray (2008) and Turchetto-Zolet et al. (2013) who
observed a bias towards vertebrate studies, 57\% and 70\% respectively.
The number of marine plants and algae studies in Brazil were quite
underrepresented (4\%) as they are in terrestrial and freshwater
autotrophic species in South America (1\% algae in Turchetto-Zolet et
al., 2013), terrestrial and marine plants in eastern North America (11\%
in Soltis et al., 2006) and world widely in general (2\% reported in
Beheregaray 2008). In the past, the disparity between the number of
phylogeographic studies between heterotrophic x autotrophic species was
attributed in part to the faster mutation rates observed in animal
markers (mitochondrial genome) compared to markers available for plant
studies (Soltis et al., 2006). An increase in the number of studies
addressing macroalgal phylogeography would improve our understating of
population genetic histories and marine phylogeography considering they
are poorly-dispersers (Kinlan \& Gaines, 2003), potentially being able
to identify a larger number of local and regional BGF and concordant
phylogeographic patterns.

The first study using genotypic data addressing the phylogeography of a
Brazilian marine species was published in 1998 (Secchi et al., 1998), 11
years after the Avise's seminal 1987 publication. Before 1998, the only
six phylogeographic studies (= four articles) addressing Brazilian
marine biota used phenotypic (isozyme) data. In Brazil mitochondrial
genotypic data started being utilized first in the form of
fragment-based methods (e.g. Secchi et al., 1998). Between 2007-2010,
RAPD, AFLP, RFLP and similar fragment-based techniques played an
important role increasing the number of publications. Microsatellites
remain a poorly used technique with only 29 studies (12\%) published
since 2001 (Beheregaray \& Sunnucks, 2001). A similar pattern was
observed for genome-wide techniques, such as SNPs, where only one marine
study was published to date (Siccha-Ramirez et al., 2018). In the world,
genome wide SNP and high-throughput DNA sequencing techniques are
becoming the powerhouse in phylogeographic studies (e.g. ddRadseq, B.
Peterson, Weber, Kay, Fisher, \& Hoekstra, 2012).

The two most well sampled and phylogeographically well studied
geopolitical states were Rio de Janeiro and São Paulo, which happens to
be the two richest states and the ones that hold the largest number of
research universities in the country, followed by Bahia (the state with
the longest coastline). The relationship between number of
phylogeographic studies and economic affluence is a well-known worldwide
pattern in the phylogeographic literature (reported in Beheregaray,
2008; Turchetto-Zolet et al., 2013). The weaker studied regions of
Brazil are those located in the extreme northern and southern reaches of
the country, where physical accessibility is challenging. Particularly
the northernmost reaches, along the Amazonian Rainforest coastline
towards Amapá, west of Belém (48° 29' 25'' W) where nearly nothing is
known about the phylogeographic structure of any coastal marine species.
The mouth of the Amazon river is considered a strong BGF in coastal
South America but studies that attributed it to explain genetic
discontinuities used populations samples thousands of kilometers apart
across the western Atlantic Ocean (e.g. Caribbean versus Brazilian
population (see de Souza et al., 2015; Nauer et al., 2019; Santos,
Hrbek, Farias, Schneider, \& Sampaio, 2006).

Linear model

The \emph{lm} identified a significant latitudinal gradient in BGF
frequency distribution along the Brazilian coast. A significant negative
correlation between BGF frequency and latitude was observed. The number
of BGF within a given region, represented here as the frequency of
putative BGF concordances across multiple taxa and markers per site,
tend to decrease as latitude increases. This result concurs with one of
the most ubiquitous large-scale biotic pattern on Earth,
the\emph{latitudinal gradient in species diversity} (LGD). Several
hypotheses have been proposed and a plethora of papers, text books and
reviews have been published, to explain the causes of LGD

(e.g. Fine, 2015; Pianka, 1966; Stevens, 1989). To make matters more
complicated, our latitude BGF gradient can be both, a result of
particular drivers used to explain LGD (e.g. climate stability,
available energy, temperature, body size, metabolic rate) and as a
driver itself (confounded with other hypotheses such as the `higher
spatial heterogeneity' hypothesis, Pianka, 1966). As a driver, all other
factors being equal, our ``BGF concentration hypothesis'' predict that a
greater number of BGF in a particular location would inevitably drive
higher species diversity across evolutionary time.

Jablonski, Huang, Roy, \& Valentine (2017) over-simplistically
classified LGD hypotheses into two non-mutually exclusive
categories:\emph{in situ} hypotheses (also known as the `producer
hypothesis') and spatial dynamics hypotheses (also known as the
`receiver hypothesis') (se also Stebbins, 1974). The former category
suggests that causes for higher species diversity in lower latitudes are
driven by local environmental factors driving higher speciation. The
latter category suggests that higher species diversity in the tropics is
driven by the arrival and concentration of species arising elsewhere
(e.g. temperate regions). Our results support the theory that speciation
rates are higher at lower latitudes not only due to factors related to
species' intrinsic biology such as smaller body size, faster metabolic
rates and shorter life cycles (Fine, 2015) but also due to the
occurrence of higher frequency of BGF in lower latitudes -- an \emph{in
situ}hypothesis. According to our data, higher BGF frequency in lower
latitudes tend to produce more genetically structured populations, which
in due time give rise to different species locally. Additionally, our
results also help identify one of the processes driving Rapoport's rule,
that species latitudinal ranges are usually smaller at lower latitudes
than at higher latitudes. Smaller latitudinal ranges between species,
particularly between sister-species and within species complexes, at
lower latitudes can be the result of higher frequency in BGF occurring
within smaller spatial scales.

We call the reader's attention to the fact that worldwide patterns of
LGD are a result of several millions of years of evolution and most of
the phylogeographic data used in this study was shaped in far smaller
time scales (\selectlanguage{english}[?] 2 million years). The extent at which higher frequency of
BGF at lower latitudes is either a recent, localized, phenomenon (i.e.
Brazil-centric) or a universal evolutionary process helping drive LGD in
the planet remains to be determined. However, marine and terrestrial
fossil records (Mittelbach et al., 2007) and, more recently, large scale
phylogenetic studies (Jablonski et al., 2017; Verbruggen et al., 2009)
suggest that higher speciation rates in lower latitudes has occurred
across geological time, worldwide.

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 Sao Roque, the easternmost promontory of the South
American continent, and the region where the South American continent
turns southward at 05deg S latitude. Cape Sao 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
oyster\emph{Crassostera} \emph{virginica} and the red alga
\emph{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 \emph{Micropogonias furnieri} (Puchnick-Legat \& Levy, 2006).
Since then several other studies have tested and detected BGF at this
region, including another crustacean (\emph{Panulirus argus:} Diniz,
Maclean, Ogawa, Cintra, \& Bentzen, 2005), six fish species (Bezerra et
al., 2018; Cortinhas et al., 2016; da Silva et al., 2016; Mendonca,
Oliveira, Gadig, \& Foresti, 2011; Montes et al., 2018; Santos et al.,
2006), some plant species (\emph{Rhizophora} spp.: Francisco, Mori,
Alves, Tambarussi, \& de Souza, 2018; Pil et al., 2011), and a turtle
species (\emph{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 (10deg S -- 20.5deg 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 (8deg 33' S) to the Abrolhos Reef Basin and
the Vitoria-Trindade seamount chain at latitude 20.5deg 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 Sao
Francisco, the Paraguacu, 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
mollusks\emph{Anomalocardia brasiliana} (Arruda, Beasley, Vallinoto,
Marques-Silva, \& Tagliaro, 2009) and the fish \emph{Rhizoprionodon
porosus} (Mendonca et al., 2011). The outflow sediment plume of the Sao
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 16deg and 20.5deg S, the continental shelf becomes
shallower and wider to form the Abrolhos Archipelago Basin and eastward
Vitoria-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
Vitoria-Trindade seamount chain (20.5deg 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
(\emph{Crassostrea} spp.: Lazoski et al., 2011), crustaceans
(\emph{Excirolana braziliensis} : Hurtado et al., 2016) and polychaete
(\emph{Perinereis} spp.: Paiva et al., 2019). The genetic
discontinuities between populations sampled north and south of the
Abrolhos Basin and the Vitoria-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 (20.5deg -- 27deg S latitude) ranges from the Vitoria-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 (\emph{Crassiphycus caudatus:} Ayres-Ostrock et al.,
2019; \emph{Hypnea pseudomusciformis} : Nauer et al., 2019), marine
vascular plants (\emph{Rhizophora} spp.: Francisco et al., 2018), a
cnidarian (\emph{Mussismilia hispida} : Peluso et al., 2018), nemerteans
(\emph{Ototyphlonemertes} spp.: Andrade, Norenburg, \& Solferini, 2011),
polychaetes (\emph{Perinereis} spp.:Paiva et al., 2019), and a sea
turtle (\emph{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 (\emph{Galeocerdo cuvier} : Carmo et al.,
2019; \emph{Macrodon atricauda} : Rodrigues et al., 2014), and a dolphin
study (\emph{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 22deg 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 \selectlanguage{english}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 (\emph{Atherinella brasiliensis} : Cortinhas et al., 2016),
crustaceans (\emph{Excirolana braziliensis} : Hurtado et al.,
2016;\emph{Litopenaeus schmitti} : Maggioni, Rogers, \& Maclean, 2003),
and a cetacean (\emph{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 Sao 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 Paranagua
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 con\selectlanguage{english}fluence
moves seasonally from 30 -- 35deg S during the winter to 40deg S -- 46deg S
during the summer (R. Peterson \& Stramma, 1991). This oceanographic
processes has been proposed a BGF (Cortinhas et al., 2016; Vasconcellos,
Lima, Bonhomme, Vianna, \& Sole-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 Vitoria-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 Sao 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
(Sao Paulo). However, the cnidarians data should be interpreted with
care, considering the low number of studies (n \textgreater{} 5).

Concluding remarks

Phylogeographic studies of the Brazilian coast is still in its infancy
when comparing to others biomes and areas of the world. To date, no
phylogeographic review have been conducted focusing on Brazilian marine
organisms. This study aimed to compile and better understand which and
how major oceanographic and geographic processes found along the
Brazilian coast could be acting as BGF. Amongst the recurrent geographic
features, the split of the Southern Equatorial Current in two at
latitude 4deg S had coincided with the largest values of phylogeographic
concordance, followed by a region characterized by the Vitoria-Trindade
seamount chain and the Doce river outflow. The Cabo Frio seasonal
upwelling system, although frequently pointed in literature as potential
strong BGF, had low phylogeographic concordance. On the other hand, the
meeting of the Malvinas' current with the Brazilian Current or the
string of estuaries in south Brazil turned out to be a region of higher
levels of BGF concordance even though such region is often not referred
as a hotspot for genetic discontinuities.

According to Fine (2015) literature review and analysis, climate
stability and the time--integrated area hypotheses alone are responsible
for all marine and terrestrial LGD patterns observed in the world. Here
we propose that a larger number of barriers to gene flow found in lower
latitudes (and the processes responsible for this pattern), together
with the climate stability and the time--integrated area hypotheses
account for LGD, at least in the marine environment.

Due to the lack of studies at the extremes of the Brazilian coast, we
could not test the effects of the Amazon river delta outflow and the Rio
Grande do Sul long unconsolidated subtract extension as geographical
BGF. Future phylogeographic papers will help improve the datasets and
consequently the models produced in this study, allowing more spatially
refined predictions of areas of high phylogeographic concordance, and
the inclusion in our analyses of putative BGF located in the extreme
northern and southern regions of Brazil.

\textbf{Acknowledgements}

This study was funded by: Coordination for the Improvement of Higher
Education Personnel (CAPES) - Finance Code 001 PhD fellowship to NTM.
Santa Catarina State Research and Innovation Support Foundation (FAPESC)
PhD fellowship to LBM. Sao Paulo Research Foundation (FAPESP)
2018/06085-1 to VC. The Brazilian National Council for Scientific and
Technological Development (CNPq), PQ2 research grants 302549/2017-0 to
VC; and 309658/2016-0 and 306304/2019-8 to CFDG, Universal grant
437115/2018-6 to CFDG. We thank the anonymous reviewers and the editor
for important comments.

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\textbf{Data Accessibility}

The data accessibility was submitted as Supplemental material.

Table S1: Data matrix built from genetic discontinuities empirical data
extracted from scientific papers published between 1987-2019 with sample
sites within the Brazilian coast

\textbf{Authors Contributions}

Conception and design of the research: NTM, VC, CFDG

Data collection and literature search: NTM, LBM, CFDG

Dataset preparation, data analysis and interpretation: NTM, LBM, VC,
CFDG

Drafting the article: NTM, LBM, VC, CFDG

\textbf{Figures captions}

Figure 1. Maps of the Brazilian coast. (A) Present time. Different
colors indicate different phylogeographic Regions I-IV. Political states
identified as their official 2-letter code. = mouth of major rivers. =
Vitoria-Trindade seamount chain. = Cabo Frio upwelling system. = Cassino
beach, the longest sandy beach in the southern hemisphere. SEC = South
Equatorial Current. (B) Current and past coastline during Pleistocene
glacial maxima with sea level 100 meters lower than present time.
Bathymetry legend corresponds to figure 1B only. Boundary current
according to R. Peterson \& Stramma (1991).

Figure 2. Number of molecular-driven marine phylogeography papers
published between 1987 and 2019 that minimally addressed Brazil's marine
biota.

Figure 3. Percentage of number of molecular-driven marine phylogeography
papers published between 1987 and 2019 that minimally addressed Brazil's
marine biota according to (A) types of genetic markers (fragment
analysis stands for ddRAD, RAPD, ISSR, AFLP, and RFLP techniques), (B)
taxonomic groups, (C) functional forms and, (D) marine habitat.

Figure 4: Generalized linear model applied of the frequency of putative
barriers to gene flow occurrences for populations of marine species
recorded along the Brazilian coast (in latitudes). Data collected from
articles contained new molecular data published between 1991 and 2019
with sample sites within the Brazilian coast.

Figure 5: Generalized additive model for the frequency of putative
barriers to gene flow occurrences for populations of marine species
sampled along the Brazilian coast. Data collected from phylogeography
papers published between 1991 and 2019. Roman numbers stands for each of
the four phylogeographic regions recognized in this model.

Figure 6: Phylogeographic break frequency at phylogeographic Regions
I-IV identified in the generalized linear model depicted in Figure 5.
The line within the box marks the median. The boundary of the box
indicates the 25\textsuperscript{th} and
75\textsuperscript{th}percentiles. Vertical line indicate the
10\textsuperscript{th} and 90\textsuperscript{th} percentiles. Whiskers
above and below the box indicate outliers outside the 10th and 90th
percentiles. Different letters above the box indicate statistically
significant differences (p \textless{} 0.05).

Figure 7: Generalized additive models for the frequency of putative
barriers to gene flow frequencies for populations of different marine
taxa recorded along the Brazilian coast. Data collected from
phylogeography papers published between 1991 and 2019 with sample sites
within the Brazilian coast. A) Fishes, B) Crustaceans, C) Mollusks and,
D) Cnidarians. Images represents an example of each taxonomic group.
Graphs were designed using resources from flaticon.com.

Table 1: Top five journals with the largest number of empirical articles
containing phylogeographic data on Brazilian marine species.\selectlanguage{english}
\begin{longtable}[]{@{}ll@{}}
\toprule
Journal & Number of articles\tabularnewline
\midrule
\endhead
PLoS ONE & 12\tabularnewline
Journal of Experimental Marine Biology and Ecology & 11\tabularnewline
Genetics and Molecular Biology & 8\tabularnewline
Marine Biology & 8\tabularnewline
Molecular Ecology & 6\tabularnewline
Total number of Journals & 74\tabularnewline
\bottomrule
\end{longtable}

Table 2: Number of studies per Brazilian geopolitical states per
taxonomic groups extracted from scientific articles published between
1987-2019.\selectlanguage{english}
\begin{longtable}[]{@{}llllllllllllllllll@{}}
\toprule
Region & North & North & Northeast & Northeast & Northeast & Northeast &
Northeast & Northeast & Northeast & Northeast & Northeast & Southeast &
Southeast & Southeast & South & South & South\tabularnewline
\midrule
\endhead
State & AP & PA & MA & PI & CE & RN & PB & PE & AL & SE & BA & ES & RJ &
SP & PR & SC & RS\tabularnewline
Ascidiacea & 0 & 0 & 0 & 0 & 0 & 0 & 0 & 0 & 0 & 0 & 0 & 2 & 4 & 4 & 1 &
3 & 0\tabularnewline
Aves & 1 & 2 & 1 & 1 & 0 & 0 & 0 & 0 & 0 & 0 & 2 & 0 & 3 & 4 & 1 & 4 &
0\tabularnewline
Cetacea & 0 & 2 & 0 & 0 & 3 & 1 & 0 & 0 & 0 & 0 & 5 & 3 & 5 & 2 & 0 & 4
& 4\tabularnewline
Cnidaria & 0 & 0 & 1 & 0 & 3 & 2 & 7 & 5 & 4 & 0 & 8 & 6 & 6 & 3 & 0 & 3
& 0\tabularnewline
Crustacea & 4 & 10 & 9 & 1 & 11 & 8 & 0 & 12 & 7 & 5 & 19 & 11 & 20 & 22
& 8 & 18 & 13\tabularnewline
Echinodermata & 0 & 0 & 0 & 0 & 0 & 0 & 0 & 0 & 0 & 0 & 0 & 0 & 4 & 0 &
0 & 0 & 0\tabularnewline
Fishes & 4 & 17 & 8 & 1 & 15 & 26 & 6 & 12 & 1 & 3 & 29 & 19 & 28 & 23 &
10 & 14 & 11\tabularnewline
Kinorhynch & 0 & 0 & 0 & 0 & 0 & 0 & 0 & 0 & 0 & 0 & 0 & 0 & 0 & 1 & 0 &
0 & 0\tabularnewline
Mollusca & 3 & 6 & 1 & 1 & 6 & 5 & 6 & 8 & 2 & 1 & 8 & 1 & 10 & 12 & 5 &
5 & 2\tabularnewline
Nemertea & 0 & 0 & 0 & 0 & 0 & 0 & 0 & 0 & 0 & 0 & 3 & 2 & 2 & 4 & 0 & 2
& 0\tabularnewline
Otariidae & 0 & 0 & 0 & 0 & 0 & 0 & 0 & 0 & 0 & 0 & 0 & 0 & 0 & 0 & 0 &
0 & 1\tabularnewline
Plantae & 0 & 6 & 4 & 3 & 4 & 3 & 1 & 4 & 0 & 1 & 4 & 2 & 2 & 4 & 3 & 3
& 0\tabularnewline
Platyhelminthes & 0 & 0 & 0 & 0 & 0 & 0 & 0 & 0 & 0 & 0 & 0 & 0 & 0 & 1
& 1 & 1 & 1\tabularnewline
Polychaeta & 0 & 0 & 0 & 0 & 3 & 0 & 2 & 3 & 0 & 0 & 1 & 3 & 2 & 3 & 2 &
0 & 0\tabularnewline
Porifera & 0 & 0 & 0 & 0 & 0 & 0 & 0 & 1 & 0 & 0 & 0 & 0 & 2 & 1 & 0 & 1
& 0\tabularnewline
Testudinata & 0 & 0 & 0 & 0 & 2 & 1 & 0 & 0 & 0 & 2 & 5 & 4 & 3 & 3 & 1
& 4 & 3\tabularnewline
Total & 12 & 43 & 24 & 7 & 47 & 46 & 22 & 45 & 14 & 12 & 84 & 53 & 91 &
87 & 32 & 62 & 35\tabularnewline
\bottomrule
\end{longtable}

Table S1: Data matrix built from genetic discontinuities empirical data
extracted from scientific papers published between 1987-2019 with sample
sites within the Brazilian coast\selectlanguage{english}
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