Biological Journal of the Linnean Society, 2011, 102, 915–929. With 2 figures Phylogenetic relationships of tropical western Atlantic snappers in subfamily Lutjaninae (Lutjanidae: Perciformes) inferred from mitochondrial DNA sequences JOHN R. GOLD1*, GARY VOELKER2 and MARK A. RENSHAW1 1Center for Biosystematics and Biodiversity, Texas A&M University, College Station, TX 77843-2258, USA 2Department of Wildlife and Fisheries Sciences and Texas Cooperative Wildlife Collections, Texas A&M University, College Station, TX 77843-2258, USA Received 18 August 2010; revised 9 November 2010; accepted for publication 9 November 2010bij_1621 915..929 Phylogenetic relationships among 20 nominal species of tropical lutjanine snappers (Lutjanidae) (12 from the western Atlantic, one from the eastern Pacific, and seven from the Indo-Pacific) were inferred based on 2206 bp (712 variable, 614 parsimony informative) from three protein-coding mitochondrial genes. Also included in the analysis were DNA sequences from two individuals, identified initially as Lutjanus apodus, which were sampled off the coast of Bahia State in Brazil (western Atlantic), and from three individuals labelled as ‘red snapper’ in the fish market in Puerto Armuelles, Panama (eastern Pacific). Bayesian posterior probabilities and maximum- likelihood bootstrap percentages strongly supported monophyly of all lutjanines sampled and the hypothesis that western Atlantic lutjanines are derived from an Indo-Pacific lutjanine lineage. The phylogenetic hypothesis also indicated that oceans where lutjanines are distributed (western Atlantic, eastern Pacific, and Indo-Pacific) are not reciprocally monophyletic for the species distributed within them. There were three strongly supported clades that included all western Atlantic lutjanines: one included six species of Lutjanus from the western Atlantic, two species of Lutjanus from the eastern Pacific, and the monotypic genera Rhomboplites and Ocyurus (western Atlantic); one that included three, probably four, species of Lutjanus in the western Atlantic; and one that included Lutjanus cyanopterus (western Atlantic), an unknown species of Lutjanus from the eastern Pacific, and three species of Lutjanus from the Indo-Pacific. Molecular-clock calibrations supported an early Miocene diversification of an Indo-Pacific lutjanine lineage that dispersed into the western Atlantic via the Panamanian Gateway. Divergent evolution among these lutjanines appears to have occurred both by vicariant and ecological speciation: the former following significant geographic or geological events, including both shoaling and closure of the Panamanian Gateway and tectonic upheavals, whereas the latter occurred via phenotypic diversification inferred to indicate adaptation to life in different habitats. Taxonomic revision of western Atlantic lutjanines appears warranted in that monotypic Ocyurus and Rhomboplites should be subsumed within the genus Lutjanus. Finally, it appears that retail mislabelling of ‘red snapper’ in commercial markets extends beyond the USA. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102, 915–929. ADDITIONAL KEYWORDS: biogeography – ecological speciation – phylogeography – vicariance. INTRODUCTION and subtropical waters (Allen, 1985). Most lutjanids are carnivorous and occur in reef- or other structure- Snappers of the perciform family Lutjanidae are associated habitats where they feed primarily on perch-like marine fishes found worldwide in tropical fishes, crustaceans, molluscs, and pelagic urochor- dates (Anderson, 2003). In addition, most lutjanids are long-lived, slow-growing, and extremely impor- *Corresponding author. E-mail: goldfi[email protected] tant to artisinal fisheries, providing a significant food © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102, 915–929 915 916 J. R. GOLD ET AL. resource for developing countries (Russ & Alcala, clade (L. griseus (L. apodus, L. jocu)) and weak to 1989; Blaber et al., 2005). Larger species in the moderate support (76% bootstrap) for a clade contain- family, primarily in the genus Lutjanus, also are ing L. campechanus and L. vivanus. Equally weak to highly sought by recreational fishers, particularly in moderate support (70% bootstrap) was obtained for a the Caribbean region, including the Gulf of Mexico group that contained 13 of the 14 lutjanids surveyed; (Allen, 1985). The family itself consists of more than Lutjanus cyanopterus fell outside this group. Different 120 species, the majority of which are found in the relationships were suggested by a search that used Indo-Pacific region and in the subfamily Lutjaninae weights derived from average consistency indices for (Allen, 1985). Eighteen lutjanid species (in six genera, characters. Rodríguez-Santiago (2008) used 405 char- three subfamilies) occur in tropical and subtropical acters (base pairs and gaps) of the 12S rRNA gene to waters of the western Atlantic Ocean. Most of these generate both Neighbour-joining (NJ) and Bayesian (three genera, 13 species) are placed in the subfamily topologies for 15 lutjanids found in the Caribbean Lutjaninae, which includes two monotypic genera Sea, including representatives from all three subfami- (Ocyurus and Rhomboplites) and 11 species in the lies. Strong support (93% bootstrap, 5000 replicates, genus Lutjanus. The other subfamilies occurring in in the NJ topology; 97% posterior probability in the the region are Etelinae (two genera, four species) and Bayesian topology) was recovered only for the L. gri- Apsilinae (one genus, one species). seus group (L. griseus, L. jocu, L. apodus). Weak to Phylogenetic relationships among western Atlantic moderate support (77% bootstrap, NJ topology; 69% lutjanines are not well established, in part because of posterior probability, Bayesian topology) was recov- morphological and behavioral similarities within the ered for a group that included the nine species of group (Sarver, Freshwater & Walsh, 1996), and in Lutjanus (including L.cyanopterus) examined, Rhom- part because of occurrence of both interspecific and boplites, and Ocyurus. Other less well supported rela- intergeneric hybrids (Domeier & Clarke, 1992). Rivas tionships were suggested. (1966) and Vergara (1980), based on morphological In the present study, we present phylogenetic characters, proposed three phenetic groups within the analyses of 20 nominal lutjanine species (12 from the assemblage: the Lutjanus griseus group (L. griseus, western Atlantic, one from the eastern Pacific, and Lutjanis apodus, Lutjanis jocu, and Lutjanis cyan- seven from the Indo-Pacific) based on DNA sequence opterus); the Lutjanis synagris group (L. synagris and data from the mitochondrial protein-coding genes Lutjanis mahagoni); and the Lutjanus analis group NADH dehydrogenase 4 (ND-4), cytochrome c oxidase (L. analis, Lutjanis campechanus, Lutjanis pur- I (COI), and cyt b. Three other lutjanids from the pureus,andLutjanis vivanus). They differed on place- western Atlantic, Etelis oculatus, Pristipomoides ment of Lutjanis buccanella, with Rivas (1966) aquilonaris (Etelinae), and Apsilus dentatus (Apsili- placing it in the L. analis group, whereas Vergara nae), were included in the analysis as outgroups to (1980) placed it in the L. synagris group. Chow & Lutjaninae, based on the phylogenetic hypothesis Walsh (1992) used allozymes and skull morphometry (Etelinae (Apsilinae, Lutjaninae) of Johnson (1980). to assess similarities among seven of these species. Sequences from species in the Indo-Pacific were Using the unweighted pair group method with arith- obtained from GenBank. Also included in the analysis metic mean, clustering of the allozyme data sup- were DNA sequences from two individuals, identified ported phenetic similarity between L. griseus and as L. apodus, which were sampled in 1998 off the L. apodus and between L. analis and L. vivanus, coast of Bahia State in Brazil, and from three indi- with L. synagris being more similar to the L. analis/ viduals labelled as ‘red snapper’ in the fish market in L. vivanus pair; monotypic Ocyurus (chrysurus)was Puerto Armuelles, Panama. Puerto Armuelles is a city more similar to the species of Lutjanus than was on Panama’s Pacific Coast in the western province of monotypic Rhomboplites (aurorubens). A comparison Chiriqui. One described lutjanine from the western of skull morphometry, however, indicated that Atlantic not sampled in the present study was L. pur- L. synagris was more similar to the L. griseus/ pureus, a species considered to be a close relative of L. apodus pair. Sarver et al. (1996) employed 640 the red snapper, L. campechanus. Recently, Gomes (combined) bp of the mitochondrially encoded 12S et al. (2008) presented convincing evidence, based on rRNA and cytochrome b (cyt b) genes to examine both phylogenetic and population-genetic analyses of relationships among 12 of the lutjanine species and DNA sequences from the mitochondrial D-loop, that two species (Pristipomoides aquilonaris and Etelis there is only a single, widespread species of red oculatus) placed in the lutjanid subfamiliy Etelinae snapper in the western Atlantic. In addition to phy- (Johnson, 1980). Strict consensus of three, equally logenetic assessment of western Atlantic lutjanines, parsimonious trees from maximum-parsimony analy- we also sought to assess the hypothesis of Miller & sis of unweighed sequences revealed strong support Cribb (2007) that all western Atlantic lutjanines arose (100% bootstrap, 250 replicates) for an L. griseus from an