Bathygobius soporator, AND B. GEMINATUS

Rodríguez-Rey, Ghennie T., Filho, Alfredo Carvalho, Araújo, Maria Elisabeth De & Solé-Cava, Antonio M., 2018, Evolutionary history of Bathygobius (Perciformes: Gobiidae) in the Atlantic biogeographic provinces: a new endemic species and old mitochondrial lineages, Zoological Journal of the Linnean Society 182, pp. 360-384 : 378-379

PHYLOGEOGRAPHY OF B. SOPORATOR AND B. GEMINATUS

The phylogeographic analyses revealed a similar pattern of genetic diversity for both B. soporator and B. geminatus . Both species presented deeply differentiated lineages (CAL and EA lineages for B. soporator and NWA lineage for B. geminatus ), separated from other related lineages (WA lineages) by 6–13 and 25–34 mutations for COI and cyt b, respectively ( Figs 4, 6; Supporting Information, Fig. S8). This deep divergence could indicate a relatively old partition corresponding to the major biogeographic provinces. In some reef fishes and sea urchins, for example, the deep genetic divergences observed among Atlantic biogeographic provinces (d = 2.3–12.7% for cyt b) were attributed to the presence of cryptic species within the Atlantic ( Muss et al., 2001; Carlin et al., 2003; Lessios et al., 2003; Rocha, 2004). The divergence values of the most differentiated lineages of B. soporator (median d = 2.7% for COI; median d = 4.1% for cyt b) and B. geminatus (median d = 1.8% for COI; median d = 2.7% for cyt b) are similar to those observed between cryptic species of some reef fishes, but are smaller than those found between sister species in the genus Bathygobius ( Table 1). Because of the lack of diagnostic morphological or pigmentation characters ( Tornabene et al., 2010), and the monomorphism in the nuclear genes RAG1 ( Tornabene & Pezold, 2011) and Rhodopsin (data not shown), we conservatively chose not to assign those lineages to distinct species. Genetic divergence without obvious morphological differences has been observed in the wrasse Halichoeres bivittatus between the tropical and subtropical habitats (d = 3.4% for cyt b; Rocha et al., 2005).

The two most closely related lineages (WA1 and WA2) of B. soporator and B. geminatus were also observed in sympatry throughout the tropical Western Atlantic and were separated by two COI and five to seven cyt b mutations, indicating a recent divergence ( Figs 4, 6; Supporting Information, Fig. S8). Co-existence of different mitochondrial lineages in sympatry has also been observed in reef fishes such as the surgeonfish Naso brevirostris ( Horne et al., 2008) , the coral trout Plectropomus maculatus and the snapper Lutjanus carponotatus ( Evans et al., 2010) . In each WA lineage of B. soporator , the Caribbean and Brazilian provinces shared the most common haplotype and four other central haplotypes. The central position of shared haplotypes indicates an old age for the connections between provinces. In B. geminatus , our results suggest that the lineages co-occur in the Brazilian coast and that the WA1 lineage may be restricted to the Brazilian province. However, because of the small sample sizes in the Caribbean, we cannot affirm that the WA1 lineage really does not occur in the Caribbean, as observed for the WA lineages of B. soporator .

Two primary hypotheses have been proposed to explain the high biodiversity of regions such as the Greater Caribbean: the centre of origin (CO) hypothesis and the centre of accumulation (CA) hypothesis ( Rocha et al., 2008b). The CO hypothesis proposes that species originate in the centre and disperse to the periphery, whereas the CA hypothesis proposes that diversity centres accumulate species that originated elsewhere ( Rocha et al., 2008b; Bowen et al., 2013). Therefore, under a CO hypothesis, the ancestral haplotypes should be found at the centre of diversity, and under a CA hypothesis, the ancestral haplotypes should be found in peripheral populations. In B. soporator , the ancestral haplotype was distributed in the Northwestern Atlantic ( Fig. 5A; Supporting Information, Fig. S9A), indicating a Greater Caribbean ancestor for the lineages that dispersed towards the Southern Atlantic, supporting the CO hypothesis. In contrast, the ancestral distribution of B. geminatus was in the Southwestern Atlantic ( Fig. 7A; Supporting Information, Fig. S9B), indicating that the lineages probably derived from a Brazilian ancestor that dispersed towards the Northern Atlantic, supporting the CA hypothesis. Genetic patterns that support both or either of the hypotheses for the Greater Caribbean have also been reported in other reef fishes (e.g. Rocha et al., 2008b; Castellanos-Gell et al., 2012), indicating that these two models are not mutually exclusive, but instead may operate in concert.

Recent phylogeographic and demographic studies have shown that climatic fluctuations during the Pleistocene (c. 2.6 Mya to 10 ka) influenced the demographic history and distribution of several marine species (e.g. Bowen et al., 2006; Rodríguez-Rey et al., 2013). During those periods, coral reef habitats experienced massive fluctuations in distribution and quality because of changes in sea level and temperature ( Daly, 1915; Kiessling et al., 2012). Reef habitats may have been reduced by 90% in the Caribbean during the glacial periods, when the sea level was at least 100 m below current levels, decreasing the available habitats for reef fishes and the connectivity among populations ( Bellwood & Wainwright, 2002; Bowen et al., 2006). During interglacial periods, the rising sea level increased habitat availability, resulting in population expansions of marine species ( Bowen et al., 2006). Our results indicate that the expansions observed in the lineages of both species of Bathygobius could have occurred during interglacial periods in Late Pleistocene (MIS5 and MIS3; Figs 5B and 7B). Thus, during those interglacial periods, the sea-level rise may have weakened the Amazon barrier (see the discussion below), increasing habitat availability and allowing the dispersal from Caribbean to Brazil for B. soporator and from Brazil to the Caribbean for B. geminatus . Demographic expansion events have also been detected during interglacial periods in several reef fishes in the Atlantic [e.g. in the squirrelfishes Myripristis jacobus and Holocentrus ascensionis ( Bowen et al., 2006) ; in the sand goby Pomatoschistus minutes ( Gysels et al., 2004; Larmuseau et al., 2009)].