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Molecular Phylogeny of the Western Atlantic Species of the Genus Portunus (Crustacea, Brachyura, Portunidae)

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Molecular Phylogeny of the Western Atlantic Species of the Genus Portunus (Crustacea, Brachyura, Portunidae) Blackwell Publishing LtdOxford, UKZOJZoological Journal of the Linnean Society0024-4082The Lin- nean Society of London, 2007? 2007 1501 211220 Original Article PHYLOGENY OF PORTUNUS FROM ATLANTICF. L. MANTELATTO ET AL. Zoological Journal of the Linnean Society, 2007, 150, 211–220. With 3 figures Molecular phylogeny of the western Atlantic species of the genus Portunus (Crustacea, Brachyura, Portunidae) FERNANDO L. MANTELATTO1*, RAFAEL ROBLES2 and DARRYL L. FELDER2 1Laboratory of Bioecology and Crustacean Systematics, Department of Biology, FFCLRP, University of São Paulo (USP), Ave. Bandeirantes, 3900, CEP 14040-901, Ribeirão Preto, SP (Brazil) 2Department of Biology, Laboratory for Crustacean Research, University of Louisiana at Lafayette, Lafayette, LA 70504-2451, USA Received March 2004; accepted for publication November 2006 The genus Portunus encompasses a comparatively large number of species distributed worldwide in temperate to tropical waters. Although much has been reported about the biology of selected species, taxonomic identification of several species is problematic on the basis of strictly adult morphology. Relationships among species of the genus are also poorly understood, and systematic review of the group is long overdue. Prior to the present study, there had been no comprehensive attempt to resolve taxonomic questions or determine evolutionary relationships within this genus on the basis of molecular genetics. Phylogenetic relationships among 14 putative species of Portunus from the Gulf of Mexico and other waters of the western Atlantic were examined using 16S sequences of the rRNA gene. The result- ant molecularly based phylogeny disagrees in several respects with current morphologically based classification of Portunus from this geographical region. Of the 14 species generally recognized, only 12 appear to be valid. We rec- ommend that P. vossi be hereafter regarded as a junior synonym of P. spinimanus and that P. bahamensis be regarded as a junior synonym of P. depressifrons. Our analysis suggests that western Atlantic members of the genus can be subdivided into at least three well-defined clades. Pending further molecular analyses with a large subset of species, it appears that the genus is not monophyletic and that it warrants further taxonomic revision. © 2007 The Linnean Society of London, Zoological Journal of the Linnean Society, 2007, 150, 211–220. ADDITIONAL KEYWORDS: Decapoda – molecular systematics – swimming crab – 16S rRNA gene. INTRODUCTION P. spinicarpus (Stimpson, 1871); P. spinimanus Latreille, 1819; P. rufiremus Holthuis, 1959; P. sebae Swimming crabs of the genus Portunus are considered (H. Milne Edwards, 1834); P. ventralis (A. Milne- ubiquitous representatives of the portunid fauna in Edwards, 1879); and P. vossi Lemaitre, 1991. Varied tropical and subtropical waters, and over 80 species diagnostic summaries and key characters based on (compiled from Rathbun, 1930; Stephenson & Camp- adult morphology, along with compilations of distribu- bell, 1959; Stephenson, 1962, 1972; Stephenson & tion records, are available in widely cited literature Rees, 1967) have been assigned to this genus world- (Rathbun, 1930; Holthuis, 1959, 1969; Williams, 1984; wide. Under present systematic treatments, 14 species Manning & Chace, 1990; Lemaitre, 1991; Melo, 1996). of Portunus have been currently recognized from the Despite the economic and ecological importance of western Atlantic: P. anceps (de Saussure, 1858); portunid species included in this commonly encoun- P. bahamensis Rathbun, 1930; P. binoculus Holthuis, tered genus, definitive identification of many species 1969; P. depressifrons (Stimpson, 1859); P. floridanus remains difficult. Diagnoses are often based on subtle Rathbun, 1930; P. gibbesii (Stimpson, 1859); and inconsistent differences in adult morphology for P. ordwayi (Stimpson, 1860); P. sayi (Gibbes, 1850); this supposedly well-known group of swimming crabs. Thus, questions remain as to the validity of several species reported in the literature, while there is also a *Corresponding author. E-mail: fl[email protected] clear possibility that yet-to-be-named species continue © 2007 The Linnean Society of London, Zoological Journal of the Linnean Society, 2007, 150, 211–220 211 212 F. L. MANTELATTO ET AL. to go unrecognized. To date, most systematic studies Specimens from both collections and also from the have been based solely on morphology, and molecular Zoology Museum of the University of São Paulo tools have been rarely applied to solve questions of (MZUSP) were loaned and used for morphological species status or to determine lower level phylogenetic comparisons. Tissues from type materials, excised by relationships (Morrison et al., 2002) within this group. minimally destructive methods, were sequenced when We herein analyse phylogenetic relationships among possible (see Table 1). all species of Portunus from the western Atlantic Ocean Besides the 16 species of Portunus, and the recently on the basis of partial sequences of the large-subunit segregated Laleonectes vocans, we included several 16S rRNA gene. Our analyses also allow us to inves- species representing other genera of the family Por- tigate the taxonomic status of several species erected tunidae for comparison, to root the analysis more on the basis of morphological characters that have broadly. These consisted of four species of Callinectes, proven difficult to apply with confidence. We include one species of Arenaeus and two species of Scylla as the genus Laleonectes to test molecular support for its additional representatives of the subfamily Portuni- separation from Portunus, as well as the proximity of nae, along with two species of Ovalipes and a species its relationship to selected members of Portunus among of Polybius to represent the subfamily Polybiinae. which it was formerly placed. Some of the comparative sequences included in the analysis were retrieved from GenBank (Table 1). DNA extraction, amplification and sequencing pro- MATERIAL AND METHODS tocols follow Schubart et al. (2000a) with modifications We based our phylogenetic analysis exclusively on a as in Mantelatto et al. (2006) and Robles et al. (2007). partial fragment of the 16S rRNA gene. Mitochondrial Total genomic DNA was extracted from muscle tissue DNA (mtDNA) is a common choice for both population of walking legs or the chelipeds. Muscle was ground and phylogenetic studies based on several character- and incubated for 1–12 h in 600 µL lysis buffer at istics such as being homoplasmic, maternally inher- 65 °C; protein was separated by addition of 200 µL ited (with some exceptions), subject to a high mutation 7.5 M ammonium acetate prior to centrifugation. DNA rate, easy to isolate and abundant (Avise et al., 1987; precipitation was made by addition of 600 µL cold Hartl & Clark, 1997; Rokas, Ladukakis & Zourus, isopropanol followed by centrifugation; the resultant 2003). Absence of recombination might represent a pellet was washed with 70% ethanol, dried and resus- limitation because mtDNA linear evolutionary history pended in 10–20 µL TE buffer. can differ from that of the nuclear DNA, which pre- An approximately 560-bp region of the 16S rRNA sents a reticulate evolutionary history (Neigel & gene was amplified from diluted DNA by means of Avise, 1986). The 16S rRNA gene has nonetheless polymerase chain reaction (PCR) (thermal cycles: ini- shown its utility in both phylogenetic and population tial denaturation for 10 min at 94 °C; annealing for studies for over a decade (Bucklin, Frost & Kocher, 38–42 cycles: 1 min at 94 °C, 1 min at 45–48 °C, 2 min 1995; Schubart, Neigel & Felder, 2000a; Stillman & at 72 °C; final extension of 10 min at 72 °C) with the Reeb, 2001; Schubart, Cuesta & Felder, 2002; Tudge following primers: 16Sar (5′-CGCCTGTTTATCAA & Cunningham, 2002; Harrison, 2004; Machordom & AAACAT-′), 16Sbr (5′-CCGGTCTGAACTCAGATCAC Macpherson, 2004; Morrison, Rios & Duffy, 2004; GT-3′), 16SH4 (5′-GTYGCCCCAACCAAATAAA-3′), Mantelatto et al., 2006; Robles et al., 2007), and it is a 16SL2 (5′-TGCCTGTTTATCAAAAACAT-3′), 16SL15 common choice for use in phylogenetic studies on deca- (5′-GACGATAAGACCCTATAAAGCTT-3′) (for refer- pods (Schubart, Neigel & Felder, 2000a; Mathews ences on the primers see Schubart, Neigel & Felder, et al., 2002; Harrison, 2004; Machordom & Macpher- 2000a and Schubart, Cuesta & Rodriguez, 2001b). We son, 2004; Morrison, Rios & Duffy, 2004). used internal primers 16SH4 and 16SL15 (in combi- Crabs used in our analyses were collected from new nation with 16SL2, 16Sar and 16Sbr) for partial localities between 2000 and 2001 or were obtained amplification of the possibly formalin-fixed specimens from museum collections (Table 1). Newly collected among museum materials. PCR products were puri- specimens to be used for DNA analysis were preserved fied using Microcon 100 filters (Millipore Corp.) and directly in 75–90% ethanol. Species identifications sequenced with the ABI Big Dye Terminator Mix (PE were confirmed on the basis of morphological charac- Biosystems) in an ABI Prism 3100 Genetic Analyser ters from available references (Rathbun, 1930; Holth- (Applied Biosystems automated sequencer). All se- uis, 1959, 1969; Williams, 1984; Manning & Chace, quences were confirmed by sequencing both strands. 1990; Lemaitre, 1991). Genetic vouchers from which A consensus sequence for the two strands was ob- tissue subsamples were obtained are deposited at the tained using the computational program Sequencher University of Louisiana-Lafayette Zoological Collec-
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