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Bathygobius Soporator Journal of Experimental Marine Biology and Ecology 320 (2005) 211–223 www.elsevier.com/locate/jembe Genetic detection of cryptic species in the frillfin goby Bathygobius soporator D. Limaa, J.E.P. Freitasb, M.E. Araujoc, A.M. Sole´-Cavaa,T aLaborato´rio de Biodiversidade Molecular; Departamento de Gene´tica, Instituto de Biologia, Universidade Federal do Rio de Janeiro, Cidade Universita´ria, CCS, Bloco A, 21941-470 Rio de Janeiro, RJ, Brazil bTropical Marine Ichthyology Group (Ictiologia Marinha Tropical-IMAT), Departamento de Engenharia de Pesca, Universidade Federal do Ceara´, Campus do Pici, Fortaleza, CE, Brazil cOceanography Department, CTG, Universidade Federal de Pernambuco, 50740-550 Recife, PE, Brazil Received 9 October 2004; received in revised form 12 December 2004; accepted 26 December 2004 Abstract We compared, through allozyme and cytochrome b sequence analyses, populations of Bathygobius soporator from four localities on the Brazilian coast with those from the Oceanic Islands of the Rocas Atoll (230 km off the Brazilian coast) and the Bahamas (5700 km northwest from Rocas). The population from the Rocas Atoll was genetically more similar to the geographically distant Bahamas (gene identity, I=0.92) than to the supposedly conspecific populations from the Brazilian coast (Ib0.55). Five diagnostic allozyme loci and a high level of nucleotide divergence (Kimura 2-parameters=0.21) were found between the two groups, further confirming that they must belong to different biological species. Since the type locality of B. soporator is in the Caribbean, the binomial should be maintained for the Bahamas/Rocas Atoll populations, and the other Brazilian populations of Bathygobius analysed either represent the occurrence of a species of Bathygobius hitherto not cited for the Brazilian coast, or belong to a new species. The coastal populations of this species were also found to be highly structured ( FST=0.18; pb0.05), indicating that, even along the coast, levels of gene flow of this species are limited. This could be related to their reproductive biology (adhesive benthic eggs with parental care and short length of larval life). The timings of the divergence between the Caribbean and the Southwest Atlantic species found here, estimated from allozymes and cytb sequences, are very similar (around 10 MY bp), and correlate with the start of the Amazon river outflow. The colonization of the Rocas Atoll by populations from the Caribbean seems to have taken place after the Caribbean and the Brazilian coast species had diverged. D 2005 Elsevier B.V. All rights reserved. Keywords: Allozymes; Atlantic Ocean; Biogeography; Cytochrome b; Fish; Mitochondrial 1. Introduction T Corresponding author. Tel.: +55 21 2562 6389; fax: +55 21 2562 6397. The frillfin goby Bathygobius soporator (Valenci- E-mail address: [email protected] (A.M. Sole´-Cava). ennes, 1837) is a bottom-dwelling species that lives in 0022-0981/$ - see front matter D 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.jembe.2004.12.031 212 D. Lima et al. / J. Exp. Mar. Biol. Ecol. 320 (2005) 211–223 tidal pools on coastal regions and oceanic islands on show the existence of two different species within both sides of the Atlantic. In the West Atlantic, it what was originally identified as B. soporator. occurs from the Florida Keys (Caribbean) to Santa Catarina (South Brazil) (Cervigo´n, 1966; Miller and Smith, 1989). In the East Atlantic, B. soporator has 2. Materials and methods been reported from the African coast from Senegal to Angola (Cervigo´n, 1966; Miller and Smith, 1989; 2.1. Sample collections Afonso et al., 1999). Four other species of this genus are found in the Atlantic Ocean: Bathygobius curacao Ninety one samples of B. soporator were and Bathygobius mystacium are endemic of the West collected from five localities in Brazil and one Atlantic, and Bathygobius casamancus and Bathygo- locality in the Bahamas (Fig. 1). The Bahamas (Lee bius burtoni are endemic of West Africa (Bohlke and Stocking Island—Lab beach) and Rocas Atoll (Farol Chaplin, 1993; Brito and Miller, 2001). In Brazil, B. Island—Ruı´nas do Farol beach) represent two soporator occurs along most of the coast, from the oceanic islands on the Caribbean and Brazilian north and northeast to the south (18Sto268 S), coasts, respectively. The Brazilian continental coast whereas B. mystacium is limited to the northeastern localities were Ceara´ (Fortaleza—Mucuripe beach), region (38Sto188S) (Miller and Smith, 1989; Bohlke Rio Grande do Norte (Natal—Artistas beach), and Chaplin, 1993). Paraı´ba (Joa˜o Pessoa—Cabo Branco beach) and Owing to their bottom-dwelling habits, several Rio de Janeiro (Mangaratiba—Junqueira beach). morphological characteristics, such as the body Fish identification followed Bohlke and Chaplin lateral line and some bones, are reduced or absent (1993). All specimens collected had the morpho- in some species of the Suborder Gobioidei. Thus, it is logical characters that are considered diagnostic of difficult to assess the biological diversity of gobiid B. soporator (18–20 pectoral fin rays, 37–41 lateral fishes based only on morphological characters scales, 0.12–0.14 maxilla length/standard length; (Akihito et al., 2000). Many marine species that Table 1) and different from those of B. mystacium, were considered to have large geographical distribu- B. curacao, B. burtoni and B. casamancus, the tions were found to be, under close scrutiny, other accepted species of Bathygobius in the complexes of morphologically similar, but geneti- Atlantic. The 17 fish morphologically analysed were cally distinct species (review in Knowlton, 2000). deposited at the Museu Nacional do Rio de Janeiro Hence, the supposed amphiatlantic distribution of a (MNRJ 27704–27715). species with a dlow morphologyT (sensu Van Oppen et al., 1997) and with very limited dispersal 2.2. Allozyme electrophoresis capabilities (adhesive eggs and short larval pelagic period, Tavolga, 1953; Peters, 1983) is likely to be a We analysed fragments of muscle tissue from B. taxonomical artifact. soporator from the six populations using 12.5% Molecular methods are suitable to detect sibling starch-gel allozyme electrophoresis as previously species in marine organisms (for reviews see, e.g. described (Sole´-Cava and Thorpe, 1986; Klautau et Knowlton, 1993; Thorpe and Sole´-Cava, 1994; al., 1999), using a 0.25 M Tris, 0.01 M EDTA, 0.06 M Knowlton, 2000). Hence, their use has become citrate, pH 8.0 (TC8) buffer system (Ward and common in the recognition of species boundaries Beardmore, 1977). Enzyme stain recipes were from and phylogenetic patterns in gobioid fishes (e.g. Manchenko (1994). We tested 17 enzyme systems, McKay, 1993; Miller et al., 1994; Akihito et al., from which we chose 13, based on their consistent and 2000; Chen et al., 2002; Gysels et al., 2004). In this reproducible results: Adenilate kinase (AK, Enzyme study we used allozymes and cytochrome b sequences Commission #2.7.4.3), alcohol dehydrogenase (ADH, to compare populations from six West Atlantic local- EC #1.1.1.1), alpha esterases (a-EST, EC #3.1.1.1), ities: four along the Brazilian coast and two from the glutamate dehydrogenase (GDH, EC #1.1.1.49), iso- oceanic islands of the Rocas Atoll (250 km off the citrate dehydrogenase (IDH, EC #1.1.1.42), lactate Brazilian coast) and the Bahamas. The results clearly dehydrogenase (LDH, EC #1.1.1.27), malate dehy- D. Lima et al. / J. Exp. Mar. Biol. Ecol. 320 (2005) 211–223 213 Fig. 1. Sampling sites. drogenase (MDH, EC #1.1.1.37), malic enzyme (ME, 2.3. Cytochrome b gene sequencing EC #1.1.1.40), mannose 6-phosphate isomerase (MPI, EC #5.3.1.8), phosphogluconate dehydrogenase We isolated genomic DNA from muscle tissue (PGD, EC #1.1.1.44), phosphoglucose isomerase from seven specimens, by proteinase digestion in lysis (PGI, EC #5.3.1.9), phosphoglucomutase (PGM, EC buffer (0.1 M Tris, pH 8.0, 0.05 M EDTA, 0.2 M #5.4.2.2) and superoxide dismutase (SOD, EC NaCl, 1% w/v of SDS and 3 mg of proteinase K) #1.15.1.1). followed by extraction with the phenol/chloroform Table 1 Meristic variation and body proportions of B. soporator (BS), B. mystacium (BM), B. curacao (BCu), B. burtoni (BB) and B. casamancus (BCs) Species BS BM BCu BB BCs Fin rays Pectoral 18–20a (18–21b;d; 19–21c) 18–20b; 19–20c 15–18b; 16–17c 18–20d 17–19d 1st dorsal VI–VIIa (=VIb;c;d) – – VI–VIId VId 2nd dorsal I/7–10a (b20b;c; I/7–9d) – – I/9–10d I/10–11d Ventral I/5+I/5a (I/5+I/5c;d) – – I/5+I/5d I/5+I/5d Anal I/7–10a (I/7–10d) – – I/9d I/9d Caudal 12–19a (14–15d) – – 14–15d 14–15d Pre-dorsal scales 22–24a (17–27d) – – 13–18d 14–21d Lateral scales 37–41a (37–41b;c; 33–40d) 33–36b;c 31–34b;c 33–38d 34–39d HL/SL (%) 25–33a (27–31d) – – 15–31d 24–30d HW/SL (%) 17–28a (16–18d) – – 14–17d 13–17d ML/SL (%) 12–14a (12–16b;10–14d) 9–12b 11–14b 9–11d 8–9d PF/SL (%) 22–33a (21–23d) – – 21–26d 19–26d VF/SL (%) 18–23a (19–23d) – – 21–24d 18–24d References: a—This work; b—Bohlke and Chaplin (1993);c—Murdy and Hoese (2004);d—Miller and Smith (1989). HL=head length; HW=head width; ML=maxilla length; PF=pectoral fin length; VF=ventral fin length; SL=standard length. 214 D. Lima et al. / J. Exp. Mar. Biol. Ecol. 320 (2005) 211–223 method, as described in Sambrook et al. (1989). The Sokal, 1973). This tree construction method was extracted DNA was precipitated with ethanol and chosen for the allozyme data because it has been ammonium acetate, resuspended in 50 AL of ultrapure shown to give better estimates of tree topology when water and stored at À20 8C.
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