Molecular phylogenetics of the butterflyfishes (Chaetodontidae): Taxonomy and biogeography of a global coral reef fish family

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Abstract

Marine butterflyfishes (10 genera, 114 species) are conspicuously beautiful and abundant animals found on coral reefs worldwide, and are well studied due to their ecological importance and commercial value. Several phylogenies based on morphological and molecular data exist, yet a well-supported molecular phylogeny at the species level for a wide range of taxa remains to be resolved. Here we present a molecular phylogeny of the butterflyfishes, including representatives of all genera (except Parachaetodon) and at least one representative of all commonly cited subgenera of Chaetodon (except Roa sensu Blum, 1988). Genetic data were collected for 71 ingroup and 13 outgroup taxa, using two nuclear and three mitochondrial genes that total 3332 nucleotides. Bayesian inference, parsimony, and maximum likelihood methods produced a well-supported phylogeny with strong support for a monophyletic Chaetodontidae. The Chaetodon subgenera Exornator and Chaetodon were found to be polyphyletic, and the genus Amphichaetodon was not the basal sister group to the rest of the family as had been previously proposed. Molecular phylogenetic analysis of data from 5 genes resolved some clades in agreement with previous phylogenetic studies, however the topology of relationships among major butterflyfish groups differed significantly from previous hypotheses. The analysis recovered a clade containing Amphichaetodon, Coradion, Chelmonops, Chelmon, Forcipiger, Hemitaurichthys, Johnrandallia, and Heniochus. Prognathodes was resolved as the sister to all Chaetodon, as in previous hypotheses, although the topology of subgeneric clades differed significantly from hypotheses based on morphology. We use the species-level phylogeny for the butterflyfishes to resolve long-standing questions regarding the use of subgenera in Chaetodon, to reconstruct molecular rates and estimated dates of diversification of major butterflyfish clades, and to examine global biogeographic patterns.

Introduction

Butterflyfishes are diverse and abundant marine perciform fishes that have spectacular coloration, high levels of ecological and morphological diversity, and are found on reefs throughout shallow, tropical seas. Because of these features, they have attracted the enthusiasm and inquiry of divers, scientists, and coral reef conservationists. Researchers have an enduring legacy of fascination with the butterflyfishes because they are a prominent focus for studies of feeding specialization (Ferry-Graham et al., 2001a, Motta, 1985, Motta, 1988, Motta, 1989, Sazima and Sazima, 2001), feeding ecology and resource partitioning (Cox, 1994, Pitts, 1991, Pratchett, 2005, Zekeria et al., 2002), mating behavior and pair bonding (Driscoll and Driscoll, 1988, Fricke, 1986, Hourigan, 1989, Tricas and Hiramoto, 1989, Yabuta, 1999, Yabuta, 2002), biogeography (Bellwood et al., 2004, Blum, 1989, Findley and Findley, 1989, Findley and Findley, 2001, Righton et al., 1996), color patterns (McMillan et al., 1999), and the curious, armored, tholichthys larval stage (Leis, 1989). Butterflyfishes comprise a biogeographical mixture of species, in which some are highly restricted endemics whereas others exhibit nearly circumtropical distributions. Although recent research has generated phylogenetic hypotheses using both morphological data (Ferry-Graham et al., 2001b, Smith et al., 2003) and molecular data (Hsu et al., 2007, Littlewood et al., 2004, McMillan and Palumbi, 1995) the exploration of evolutionary, ecological and biogeographic patterns remains limited by lack of a well-resolved molecular phylogeny involving species from each of the major chaetodontid clades. The present study provides a phylogenetic analysis of butterflyfishes with a wide range of taxonomic sampling, enabling the examination of evolutionary and biogeographic patterns among species groups within the family.

The most comprehensive previous study of chaetodontid phylogenetics was based on morphology (Blum, 1988). Blum’s coding and analysis of butterflyfish morphological characters persists as the most relied-upon taxonomic and phylogenetic guide. This phylogeny was constructed using composite taxa as representatives of subgenera, and a combination of features of outgroups distilled to a hypothetical ancestor. Ferry-Graham et al. (2001b) published a morphologically-based phylogeny using several character state revisions of Blum’s (1988) dissertation work. Smith et al. (2003) updated, refined, and expanded this morphological database, including new characters based on soft tissue anatomy. The resultant phylogeny strongly supported the monophyly of the Chaetodontidae, identified the major clades within the family, and proposed a topology for the branching pattern of Chaetodon subgenera.

An active area of evolutionary research on the family is the phylogenetic placement of the long-jawed butterflyfishes. This question is of interest in order to understand the evolution of several specializations of skull biomechanics in the genera Forcipiger and Chelmon. The mechanism of feeding in the long-jawed butterflyfishes has been explored from the perspectives of quantitative kinematics, morphology, and the trends in feeding that are apparent when integrated with a phylogeny (Ferry-Graham et al., 2001b). This study used the morphological phylogeny to propose a scenario for the evolution of specialized jaw protrusion in the group. Molecular evidence illuminating the evolution of this clade, however, remains an important goal for the continued exploration of ecological and evolutionary trends in this family.

Several molecular phylogenetic studies have been conducted on butterflyfishes, including analysis of the cytochrome b gene on a group of 13 Pacific species (McMillan and Palumbi, 1997). This study questioned the monophyly of the Chaetodon (Exornator) clade, finding that C. argentatus (typically placed in Chaetodon subgenus Exornator) grouped with members of the Roaopstinkeri” complex. Further, they found that Chaetodon subgenera were genetically structured by the Pacific and Indian Ocean basins rather than by subgeneric assignment. A molecular phylogeny focusing on the genus Chaetodon (Littlewood et al., 2004) and based on the Genbank data of Nelson et al. (unpublished) also conflicted in part with previous hypotheses. The results of this analysis placed Parachaetodon as sister to C. trifascialis of the C. (Megaprotodon) subgenus and found monophyly of some Chaetodon subgenera. These studies represent the first steps toward resolution of relationships within Chaetodon using molecular data, but were not able to address broad-scale questions of intrafamily relationships or species-level chaetodontid phylogeny.

The phylogenetic composition and taxonomic utility of many of the proposed generic and subgeneric groupings within the Chaetodontidae remain to be explored. Some butterflyfish systematists (Allen et al., 1998, Blum, 1988) and the authors of popular aquarist books (Kuiter, 2002) vary in the species comprising various subgenera and even genera. The current study contains representatives of all currently recognized genera and Chaetodon subgenera, with the exception of the monotypic Parachaetodon ocellatus and Roaops (sensu Blum, 1988). Phylogenetic resolution of the family will allow assessment of taxonomic subdivisions within the family, and provide a framework for reconstructing the patterns of diversification of these charismatic reef inhabitants. Our goals in this contribution are to (1) generate a phylogeny that tests species-level relationships within the family Chaetodontidae, (2) assess the phylogenetic validity of the Chaetodon subgenera, and (3) examine the relative rates of molecular evolution, dates of divergence of major groups, and biogeographic history of butterflyfishes.

Section snippets

Taxon sampling and genes sequenced

We analyzed data from 71 butterflyfishes and 13 perciform outgroups for a total of 84 taxa. Ingroup taxa were selected to maximize sampling of generic and subgeneric ranking within the Chaetodontidae. Outgroups were selected based on availability and consideration of numerous past proposals of relational proximity to the butterflyfishes. Outgroups consist of the Zanclidae, Drepaneidae, Ephippidae, Kyphosidae (including Microcanthus and Atypichthys), Scatophagidae and members of the

Results

Phylogenetic analysis resulted in a well-resolved hypothesis of relationships at the species level (Fig. 1), and the tree topology supported monophyly of the Chaetodontidae, monophyly of all butterflyfish genera, and monophyly of most but not all of the Chaetodon subgenera (Fig. 2). C. burgessi, which had been categorized as a member of subgenus Roaops, grouped within C. (Exornator) in our study, rendering it polyphyletic. Chaetodon subgenus Chaetodon (sensu Blum, 1988) was split into two

Discussion

Phylogenetic analysis of molecular data for the Chaetodontidae resulted in a robust phylogeny that agrees with previous morphological hypotheses at the level of most major clades and some of the relationships among butterflyfish genera, but disagrees with earlier work regarding the topology of relationships within Chaetodon. We use the present molecular data set to statistically test previous phylogenetic hypotheses in a Bayesian framework and to reevaluate taxonomic groupings within the

Acknowledgments

Field work for tissue collection was aided by the Lizard Island Research Station, Mark McGrouther, Jeff Leis, Randy Mooi, Tom Trinski, Jeff Williams, Kent Carpenter, Luz Regis, Keith Lapuos, Jeff Janovetz, Brad Wright, Aaron Rice, Jim Cooper, and others on expeditions to the northern Great Barrier Reef, Vanuatu, Solomon Islands, and the Philippines. Thanks also to Overnight Fish and Apet, Inc. for assistance obtaining a few taxa that were otherwise difficult to acquire. DNA sequencing was aided

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