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Molecular Phylogenetics and Evolution Historical Biogeography ARTICLE IN PRESS Molecular Phylogenetics and Evolution xxx (2008) xxx-xxx Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution ELSEVIER journal homepage: www.elsevier.com/locate/ympev Historical biogeography and speciation in the reef fish genus Haemulon (Teleostei: Haemulidae) Luiz A. Rochaab*. Kenyon C. Lindemanc, Claudia R. Rochaa, H.A. Lessiosb "University of Texas at Austin, Marine Science Institute, 750 Channel View Drive, Port Aransas, TX 78373, USA b Smithsonian Tropical Research Institute, Balboa, Panama c Department of Marine and Environmental Systems, Florida Institute of Technology, 150 W. University Blvd., Melbourne, FL 32901, USA ARTICLE INFO ABSTRACT Article history: The high biodiversity of tropical marine hotspots has long intrigued evolutionary biologists and biogeog- Received 12 November 2007 raphers. The genus Haemulon (grunts) is one of the most important (numerically, ecologically, and eco- Revised 20 May 2008 nomically) reef fish groups in the New World and an excellent candidate to test hypotheses of Accepted 20 May 2008 speciation and diversity generation in the Greater Caribbean, the richest Atlantic biodiversity hots pot, Available online xxxx as well as the eastern Pacific. To elucidate the phylogenetic relationships among the species of Haemulon, we obtained a combined total of 2639 base pairs from two mitochondria! genes (cytochrome b and cyto- Keywords: chrome oxidase I), and two nuclear genes (TMO-4C4 and RAG2) from all nominal species. Parsimony, Reef fish Western Atlantic Maximum likelihood, and Bayesian analyses resulted in a well-resolved phytogeny with almost identical Eastern Pacific topologies. Previous phylogenetic hypotheses based on adult morphology, such as the close relationship Biogeography among H. aurolineatum, H. boschmae, and H. striatum were not supported, whereas others using develop- Brazil mental characters, such as the relationship between H. plumieri and H. sciurus, were confirmed. Our data Caribbean also indicate that the populations of the nominal H. steindachneri from the two sides of the Isthmus of Inermia Panama are genetically divergent at the species level in each ocean, and that the boga, Inermia vittata (family Inermiidae), belongs in the genus Haemulon. This evidence implies that there are 21 valid species of Haemulon, two more than previously recognized. The Amazon barrier and the Isthmus of Panama seem to have played roles in allopatric speciation of Haemulon. However, the majority of sister species pairs have completely overlapping distributions, indicating that vicariance is not the only process driving spe- ciation in this genus. We conclude that both vicariance between biogeographic provinces, and ecological mechanisms of speciation within provinces contribute to species richness in the genus Haemulon. © 2008 Elsevier Inc. All rights reserved. 1. Introduction Pacific marine faunas, but also because it brought drastic environ- mental and oceanographic changes to the region (Jackson et al., Harboring more than 800 species of fishes, the Greater Carib- 1997; O'Dea et al., 2007). Those vicariant events, combined with bean is the most diverse marine biogeographic province of the the large environmental variation along the New World tropics New World tropics (Briggs, 1974; Rocha, 2003; Floeter et al., and the relative simplicity of the Atlantic Ocean (compared to 2008). Two major vicariant events have influenced the Greater the much more complex Indo-Pacific), make this an ideal area to Caribbean marine fauna in the last 10 million years (Myr). First, study evolution and speciation in the marine realm. the late Miocene establishment of the Amazon river outflow effec- The genus Haemulon (family Haemulidae) represents an tively separated the shallow water fauna of the Caribbean from excellent group to study evolution and speciation in the New that further south in Brazil (Rocha, 2003; and references therein). World tropics. It contains 19 nominal species distributed Second, the Pliocene rise of the Isthmus of Panama, approximately throughout the tropical eastern Pacific and western Atlantic. 3.1 Myr ago (Coates and Obando, 1996) is the geological event The evolutionary history of these species was likely influenced responsible for major changes in the New World tropical fauna, by both the Isthmus of Panama and the Amazon barrier. Because not only because it separated the Caribbean and tropical eastern they attain relatively large size and their adult stages are easy to identify visually, their alpha taxonomy is well resolved. Some species live in mid-water and feed on plankton while most live * Corresponding author. Address: University of Texas at Austin, Marine Science near the bottom and feed on macrobenthic organisms after daily Institute, 750 Channel View Drive, Port Aransas, TX 78373, USA. Fax: +1 361 749 6777. feeding migrations from the reef to soft bottom and vegetated E-mail address: [email protected] (LA. Rocha). communities (Parrish, 1989). Haemulon species display high 1055-7903/$ - see front matter © 2008 Elsevier Inc. All rights reserved. doi:l 0.1016/j.ympev.2008.05.024 Please cite this article in press as: Rocha, LA. et al., Historical biogeography and speciation in the reef fish genus Haemulon ..., Mol. Phy- logenet. Evol. (2008), doi:10.1016/j.ympev.2008.05.024 ARTICLE IN PRESS LA. Rocha et al./Molecular Phylogenetics and Evolution xxx (2008) xxx-xxx morphological diversity as adults (e.g., H. macrostomum and H. 2.2. DNA extraction, PCR amplification, and sequencing striatum), yet share extremely similar early developmental stages (Courtenay, 1961) that are often visually separable only by use Total genomic DNA was extracted from tissue samples using the of complex differences in pigmentation and squamation patterns Qjagen DNeasy tissue kit following the manufacturer's protocol. (Hong, 1977; Lindeman and Richards, 2005). Fishes of this genus Segments from two mitochondrial DNA (mtDNA) genes, cyto- numerically dominate shallow tropical reefs in the Caribbean chrome b (CytB) and cytochrome oxidase I (COI), and two nuclear and eastern Pacific (schools reaching the thousands), and com- genes, TMO 4c4 and recombination-activating gene 2 (RAG2) were prise one of the most important reef fishes in the region due amplified for all species. Primers used for amplification and to their abundance, fishery value, and trophic importance as pre- sequencing are listed in Table 2. Each PCR had a total volume of dators and prey (Meyer et al., 1983; Lindeman and Toxey, 2002; 25 u.1, containing between 1 and 2 ul (10-20 ng) of purified DNA, Ferreira et al., 2004). 2.5 ul of lOx reaction buffer, 1.5 u.1 of 8 mM pre-mixed dNTPs, Fifteen species of Haemulon are found in the western Atlantic, 2.5 mM of MgCl2, 0.25 uM of each primer and one unit of Taq and five in the eastern Pacific with one nominally shared by both DNA polymerase (Promega, Madison, WI). Cycling parameters for regions (Lindeman, 1986; Rocha and Rosa, 1999). A variety of the mtDNA were as follows: initial denaturation at 94 °C for hypotheses have been proposed regarding relationships among 2 min; 35 cycles of 94 °C for 45 s, 50 °C for 45 s, 72 °C for 55 s; some groups of species within the genus, most based on general and a final extension at 72 °C for 2.5 min. Cycling for amplification body shape and ecological preferences. These hypotheses placed of the TMO gene was identical to the mtDNA except for a 54 °C planktivore species with slender bodies together, with benthic annealing temperature. The RAG2 gene was amplified by a PCR feeding deep-bodied species in other groups (Courtenay, 1961, consisting of an initial denaturation at 94 °C for 2 min followed 1965; Davis, 1967; Lindeman, 1984). However, despite their abun- by two sets of cycles: first, nine cycles of 94 °C for 45 s, 56 °C for dance, economic importance, trophic significance, and ecomorpho- 45 s, 72 °C for 55 s; second, 29 cycles of 94 °C for 45 s, 53 °C for logical diversification, no comprehensive phylogenetic analysis of 45 s, 72 °C for 1 min 45 s; and a final extension at 72 °C for the genus has been conducted. 5 min. Excess oligonucleotide primers in all cases were removed Here we present and discuss the results of a phylogenetic anal- through simultaneous incubation of PCR product with exonuclease ysis of all 19 nominal species of the genus Haemulon based on two I and shrimp alkaline phosphatase (USB Corp., Cleveland, OH). mitochondrial (cytochrome b and cytochrome oxidase I) and two Double stranded cycle sequencing reactions were conducted nuclear (TMO 4c4 and recombination-activating gene 2) genes. using dye-labeled terminators (ABI Prism technology) and the Specifically, we address the following questions: How did the Ama- amplification primers. The resulting products were separated on zon and the Isthmus of Panama barriers influence speciation in an ABI 3700 DNA sequencer (Applied Biosystems, Inc., Foster City, Haemulon? Is the geminate species status of three pairs of Haemu- CA) in DNA sequencing facilities at the Smithsonian Tropical Re- lon separated by the Isthmus of Panama (Jordan, 1908; Thomson et search Institute and the University of Hawaii. All samples were se- al., 1979) supported by molecular data? Are the previous morpho- quenced in the forward and reverse directions to verify nucleotide logical hypotheses of natural groups within Haemulon (Courtenay, designations. 1961,1965; Davis, 1967; Lindeman, 1984) supported by molecular data? What can new information on the complex phytogeny and
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