Phylogenetic relationships and evolutionary history
of the reef Wsh family Labridae
Mark W. Westneat a,¤, Michael E. Alfaro a,b
a Department of Zoology, Field Museum of Natural History, Chicago, IL 60605-2496, USA
b School of Biological Sciences, Eastlick Hall, Room 277, P.O. Box 644236, Washington State University, Pullman, WA 99164-4236, USA Received 23 October 2004; revised 5 February 2005
The family Labridae (including scarines and odacines) contains 82 genera and about 600 species of Wshes that inhabit coastal and continental shelf waters in tropical and temperate oceans throughout the world. The Labridae (the wrasses) is the Wfth largest Wsh family and second largest marine Wsh family, and is one of the most  orphologically and ecologically diversiWed families of Wshes in size, shape, and color. Labrid phylogeny is a long-standing problem in ichthyology that is part of the larger question of relationships within the suborder Labroidei. A phylogenetic analysis of labrids was conducted to investigate relationships among the six classical tribes of wrasses, the aYnities of the wrasses to the parrotWshes (scarines), and the broad phylogenetic structure among labrid genera. Four gene fragments were sequenced from 98 Wsh species, including 84 labrid Wshes and 14 outgroup taxa. Taxa were  chosen from all major labrid clades and most major global ocean regions where labrid Wshes exist, as well as cichlid, pomacentrid, and embiotocid outgroups. From the mitochondrial genome we sequenced portions of 12S rRNA (1000 bp) and 16S rRNA (585 bp), which were aligned by using a secondary structure model. From the nuclear genome, we sequenced part of the protein-coding genes RAG2 (846 bp) and Tmo4C4 (541 bp). Maximum likelihood, maximum parsimony, and Bayesian analyses on the resulting 2972 bp of DNA sequence produced similar topologies that conWrm the monophyly of a family Labridae that includes the parrotWshes and butterWshes and strong support for many previously identiWed taxonomic subgroups. The tribe Hypsigenyini (hogWshes, tuskWshes) is the sister group to the remaining labrids and includes odacines and the chisel-tooth wrasse Pseudodax moluccanus, a species  previously considered close to scarines. Cheilines and scarines are sister-groups, closely related to the temperate Labrini, and pseudocheilines and cheilines are split in all phylogenies. The razorWshes (novaculines) and temperate pseudolabrines form successive sister clades to the large crown group radiation of the Julidini. The cleaner wrasses (Labrichthyini) are nested within this radiation and several julidine genera do not appear to be monophyletic (e.g., Coris and Halichoeres). Invasion of temperate water by this predominantly tropical group has occurred multiple times and the reconstruction of biogeography assuming an Indo-PaciWc ancestor results in Wve diVerent lineages invading the Atlantic/Caribbean region. Functional novelties in the feeding apparatus have allowed labrid Wshes to occupy nearly every feeding guild in reef environments, and trophic variation is a central axis of diversiWcation in this family.
2005 Published by Elsevier Inc.
Keywords: Labridae; Reef Wshes; Phylogeny; Mitochondrial DNA; Nuclear DNA; Biogeogeraphy; Functional morphology

A central goal of ichthyology is to resolve phylogenetic relationships within and among the largest families
of marine reef Wshes. Shallow-water reef Wshes have undergone major species radiations and are a large part of the vertebrate diversity of the world’s oceans. Biologically diverse and species-rich families of reef Wshes such as gobies, blennies, wrasses, groupers and their relatives are increasingly being studied with molecular phylogenetic tools in order to answer taxonomic, phylogenetic, and evolutionary questions. The family Labridae, the wrasses, are a diverse group of over 600 Wsh species in 82genera that vary in body shape, size, coloration, and habitat (Parenti and Randall, 2000; Westneat, 1999).

Most species are small, attaining a body length of less than 20 cm, although several species attain a mass of over 100 kg. Labrids inhabit tropical marine and temperate waters around the world, and are most common in shallow water habitats such as coral reefs, rocky reefs, sand, grass, and algae. Feeding habits in the group are diverse, including gastropods, bivalves, crustaceans, Wshes, coral mucous, zooplankton, ectoparasites, and algae. The structural and ecological diversity of labrids has attracted the attention of biologists studying the ecology, life history, and biomechanics of the family.

Although phylogenetic hypotheses for many sub-groups of the Labridae have recently been proposed (Barber and Bellwood, 2005; Clements et al., 2004; Hanel et al., 2002; Streelman et al., 2002) a higher-level phylogeny for the family has not been developed. The present study proposes a phylogeny for most genera and all major clades of the family Labridae and uses the phylogeny to interpret the biogeographic and evolutionary history of the family.

The Labridae are traditionally classiWed in the suborder Labroidei with the families Scaridae, Odacidae, Cichlidae,Pomacentridae, and Embiotocidae (Greenwood et al., 1966). However, considerable uncertainty remains regarding the relationships among these groups and the accuracy of grouping these six families together (Kaufman and Liem, 1982; Liem and Greenwood, 1981; Stiassny and Jensen, 1987). Stiassny and Jensen (1987) concluded that the Labroidei is monophyletic but that extensive homoplasy exists among labroid morphological character states. They suggested that Labridae and Pomacentridae were sister-groups, with Embiotocidae sister to them and Cichlidae as the basal labroid family.

On the other hand, Streelman and Karl (1997) used the single copy Tmo4C4 nuclear DNA locus to suggest that the Labroidei are not monophyletic, but that pomacentrids and embiotocids are allied with more basal perciforms. In designing our study we sampled disparate taxa from each of the labroid subfamilies to capture the range of diversiWcation within these subclades and provide a comprehensive outgroup structure for the Labridae. Early attempts to classify labrid Wshes date to the work of Günther (1861) and Bleeker (1862). Günther (1861) recognized a single family Labridae that included scarids (parrotWshes) and odacids (rock whitings, rainbowWsh) and divided it into six groups. Bleeker (1862)
deWned ten subgroups within the Labridae, after removing the scarids. Gill (1893) included 11 subfamilies in the Labridae. Jordan and Snyder (1902) reviewed the labroid Wshes of Japan, recognizing three labroid families:
Pomacentridae, Labridae, and Scaridae. Regan (1913) and Norman (1966) recognized nine labrid subfamilies, whereas Jordan (1923) excluded Scaridae and Odacidae from the labrids and divided the labrids into three families: Labridae, Coridae, and Neolabridae. Currently, a family Labridae with six tribes is recognized based on the work of Gomon (1997) and Russell (1988). Gomon (1997) proposed a phylogenetic hypothesis for the tribe Hypsigenyini. Russell (1988) identiWed six tribes as labrid subgroups, including the Hypsigenyini,Labrini, Cheilinini, Novaculini, Labrichthyini, and Julidini and published the Wrst cladistic hypothesis for a labrid subgroup, resolving a species tree for the “pseudolabrine” group within the Julidini. Bellwood (1994) resolved generic scarid relationships and showed that the parrotWshes are nested within the Labridae, proposing that the monotypic genus Pseudodax was the sistergroup to the scarids. Westneat (1993) resolved relationships for the tribe Cheilinini and suggested a sister-group pair of cheilines and pseudocheilines and a close relationship of the Cheilinini to the temperate, mostly Eastern Atlantic tribe Labrini. Using molecular phylogenetic approaches, hypotheses have been proposed for the genus Sparisoma among the parrotWshes (Bernardi et al., 2000), for relationships among parrotWshes at the genus level (Streelman et al., 2002), among species in the tribe Labrini (Hanel et al., 2002), within the temperate odacine lineage that is nested within the labrid tribe Hypsigenyini (Clements et al., 2004), and most recently, for the genus Halichoeres (Barber and Bellwood, 2005).

Major questions remain at virtually all levels of labrid phylogeny. Rapid progress in resolving the phylogeny, classiWcation, and evolutionary biology of this large family demands a higher-level tree that shows relationships of major groups and begins to test monophyly of labrid subclades. Here, we analyze nucleotide sequences for mitochondrial and nuclear genes totaling nearly 3000 bases for 103 taxa, including 90 labrids and 13 outgroups. The central goals of this research are to propose the Wrst large scale phylogeny for the Labridae and begin interpretation of the evolutionary history of this diverse reef Wsh family.


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