Phylogenetic relationships and evolutionary history of the reef fish family Labridae
Introduction
A central goal of ichthyology is to resolve phylogenetic relationships within and among the largest families of marine reef fishes. Shallow-water reef fishes 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 fishes 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 fish species in 82 genera 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, fishes, 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 classified 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 diversification within these subclades and provide a comprehensive outgroup structure for the Labridae.
Early attempts to classify labrid fishes date to the work of Günther (1861) and Bleeker (1862). Günther (1861) recognized a single family Labridae that included scarids (parrotfishes) and odacids (rock whitings, rainbowfish) and divided it into six groups. Bleeker (1862) defined ten subgroups within the Labridae, after removing the scarids. Gill (1893) included 11 subfamilies in the Labridae. Jordan and Snyder (1902) reviewed the labroid fishes 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) identified six tribes as labrid subgroups, including the Hypsigenyini, Labrini, Cheilinini, Novaculini, Labrichthyini, and Julidini and published the first 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 parrotfishes are nested within the Labridae, proposing that the monotypic genus Pseudodax was the sister-group 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 parrotfishes (Bernardi et al., 2000), for relationships among parrotfishes 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, classification, 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 first large scale phylogeny for the Labridae and begin interpretation of the evolutionary history of this diverse reef fish family.
Section snippets
Taxon sampling
We analyzed DNA sequence data for 98 species of fishes in this study (Table 1), including 14 outgroup taxa (four non-labroid perciform outgroups, three cichlids, three embiotocids, and four pomacentrids), and 84 members of the Labridae selected from all major taxonomic groups (tribes). All specimens were collected by the authors in their natural habitat, purchased at local fish markets, or obtained from colleagues, and most have a voucher specimen associated with the tissue sample. A total of
Results
Sequence data from four genes including both mitochondrial and nuclear loci provided excellent resolution at both higher levels and among genera and species within the Labridae. The mitochondrial and nuclear loci we studied often evolved at different rates in disparate parts of the labrid tree, and the nuclear genes had a substitution rate similar to that of 12S rRNA. Multiple methods of phylogenetic analysis produced similar topologies of relationship among the wrasses. Important findings
Discussion
Development of robust hypotheses for phylogenetic relationships within and among the major groups of coastal marine and coral reef fishes will have a major impact on our ability to analyze the evolutionary biology of these colorful, diverse and ecologically important animals. The phylogeny presented here is largely consistent with preliminary phylogenetic frameworks for the family (Westneat, 1997) and for labrid subgroup trees (Bellwood, 1994, Gomon, 1997, Russell, 1988) derived from
Acknowledgments
We thank David Bellwood (James Cook University), Terry Bertozzi (South Australian Museum), Di Bray (Museum of Victoria), Kendall Clements (University of Auckland), Mark MacGrouther (Australian Museum), Luiz Rocha (STRI), Todd Streelman (University of New Hampshire), and Peter Wainwright (UC Davis) for supplying labrid tissues. Field work was aided by the Lizard Island Research Station, Mark McGrouther, Jeff Leis, Randy Mooi, Tom Trinski, Jeff Williams, Kent Carpenter, Luz Regis, Jeff Janovetz,
References (67)
- et al.
Evolutionary dynamics of complex biomechanical systems: an example using the four-bar
Evolution
(2004) - Alfaro, M.E., Bolnick, D.I., Wainwright, P.C., 2005. Evolutionary consequences of many-to-one mapping of jaw morphology...
Systematic biology of gymnotiform and mormyriform electric fishes: phylogenetic relationships, molecular clocks and rates of evolution in the mitochondrial rRNA genes
J. Exp. Biol.
(1999)- Barber, P.H., Bellwood, D.R., 2005. Biodiversity hotspots: evolutionary origins of biodiversity in wrasses...
- et al.
The utility of the incongruence length difference test
Syst. Biol.
(2002) - et al.
Model simulation of the Cretaceous ocean circulation
Science
(1989) - Bellwood, D.R., 1990. A new fossil fish Phyllopharyngodon longipinnis gen. et sp. nov. (Family Labridae) from the...
A phylogenetic study of the parrotfishes family Scaridae (Pisces: Labroidei), with a revision of genera
Rec. Austr. Mus. Suppl.
(1994)- et al.
A review of the fossil record of the parrotfishes (Labroidei: Scaridae) with a description of a new Calotomus species from the middle Miocene (Badenian) of Austria
Ann. Naturhist. Mus. Wien
(1991) - et al.
Evolution and biogeography of marine angelfishes (Pisces: Pomacanthidae)
Mol. Phylogenet. Evol.
(2004)
The history and biogeography of fishes on coral reefs
Dating the tree of life
Science
Evolution of coral reef fish Thalassoma sp. (Labridae). 1. Molecular phylogeny and biogeography
Mar. Biol.
Molecular systematics, zoogeography, and evolutionary ecology of the Atlantic parrotfish genus Sparisoma
Mol. Phylogenet. Evol.
Conspectus generum Labroideorum analyticus
Verslag. Akad. Amsterdam
Biogeography of the Chaetodontidae: an analysis of allopatry among closely related species
Environ. Biol. Fishes
Relationships of the temperate Australasian labrid fish tribe Odacini
Mol. Phylogenet. Evol.
Can three incongruence tests predict when data should be combined?
Mol. Biol. Evol.
Basic methods in molecular biology
Confidence limits on phylogenies: an approach using the bootstrap
Evolution
Families and subfamilies of fishes
Mem. Natl. Acad. Sci.
Relationships of fishes of the labrid tribe Hypsigenyini
Bull. Mar. Sci.
A revision of the Odacidae, a temperate Australian–New Zealand labroid fish family
Indo-Pacific Fishes
Phyletic studies of teleost fishes, with a provisional classification of living forms
Bull. Am. Mus. Nat. Hist.
A preliminary synopsis of the labroid genera
Ann. Mag. Nat. Hist. Ser.
Collection of small subunit (16S and 16S-like) ribosomal RNA structures
Nucleic Acids Res.
Phylogenetic relationships, evolution of broodcare behavior, and geographic speciation in the wrasse tribe Labrini
J. Mol. Evol.
Potential applications and pitfalls of Bayesian inference of phylogeny
Syst. Biol.
Bayesian phylogenetic model selection using reversible jump Markov chain Monte Carlo
Mol. Biol. Evol.
A classification of fishes including families and genera as far as known
Stanford Pub. Biol. Sci.
A review of the labroid fishes and related forms found in the waters of Japan
Proc. U.S. Nat. Mus.
Fishes of the suborder Labroidei (Pisces: Perciformes): phylogeny, ecology and evolutionary significance
Breviora
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