doi:10.1111/j.1420-9101.2009.01904.x Evolutionary history of the butterflyfishes (f: Chaetodontidae) and the rise of coral feeding fishes D. R. BELLWOOD* ,S.KLANTEN*à,P.F.COWMAN* ,M.S.PRATCHETT ,N.KONOW*§ &L.VAN HERWERDEN*à *School of Marine and Tropical Biology, James Cook University, Townsville, Qld, Australia Australian Research Council Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Qld, Australia àMolecular Evolution and Ecology Laboratory, James Cook University, Townsville, Qld, Australia §Ecology and Evolutionary Biology, Brown University, Providence, RI, USA Keywords: Abstract biogeography; Of the 5000 fish species on coral reefs, corals dominate the diet of just 41 chronogram; species. Most (61%) belong to a single family, the butterflyfishes (Chae- coral reef; todontidae). We examine the evolutionary origins of chaetodontid corallivory innovation; using a new molecular phylogeny incorporating all 11 genera. A 1759-bp molecular phylogeny; sequence of nuclear (S7I1 and ETS2) and mitochondrial (cytochrome b) data trophic novelty. yielded a fully resolved tree with strong support for all major nodes. A chronogram, constructed using Bayesian inference with multiple parametric priors, and recent ecological data reveal that corallivory has arisen at least five times over a period of 12 Ma, from 15.7 to 3 Ma. A move onto coral reefs in the Miocene foreshadowed rapid cladogenesis within Chaetodon and the origins of corallivory, coinciding with a global reorganization of coral reefs and the expansion of fast-growing corals. This historical association underpins the sensitivity of specific butterflyfish clades to global coral decline. butterflyfishes (f. Chaetodontidae); of the remainder Introduction most (eight) are in the Labridae. Why so few species Coral reef fishes are a highly diverse group, with an have been able to exploit such a widespread resource evolutionary history extending back more than 50 Myr remains a mystery. It also highlights the exceptional (Bellwood & Wainwright, 2002). From the fossil record, abilities of the few corallivores that have managed to it appears that scleractinian-dominated coral reefs and subsist on corals, and the remarkable status of butter- modern coral reef fish families first appeared and then flyfishes. Despite being one of the most intensively diversified at approximately the same time, in the early studied families of reef fishes, the evolution of this highly Cenozoic (Bellwood, 1996; Bellwood & Wainwright, specialized feeding mode remains poorly understood. In 2002; Wallace & Rosen, 2006). This suggests that the particular, how many times has corallivory arisen within origins of modern coral reefs and their associated fish the group and when did this unusual feeding mode first families may be closely linked. However, it is remarkable arise? Did corallivory arise along with major coral groups that of the 5000 or more fish species recorded from coral in the early Eocene? reefs today only 128 eat corals (Cole et al., 2008; Rotjan & Butterflyfishes are conspicuous and iconic inhabitants Lewis, 2008) and just 41 are believed to feed directly on of coral reef environments. The family contains over 130 scleractinian corals as their primary source of nutrition. species with representatives in all coral reef regions Moreover, 61% (25 of 41) belong to a single family, the (Allen et al., 1998; Kuiter, 2002). Their colourful pat- terns, and ease of identification and observation have ensured that the behavioural, ecological, morphological Correspondence: David R. Bellwood, School of Marine and Tropical Biology, James Cook University, Townsville, Qld 4811, Australia. and biogeographic characteristics of butterflyfishes have Tel.: +61 7 4781 4447, fax: +61 7 4725 1570; been extensively studied (e.g. Motta, 1988; Ferry- e-mail: [email protected] Graham et al., 2001a; Findley & Findley, 2001; Pratchett, ª 2009 THE AUTHORS. J. EVOL. BIOL. 23 (2010) 335–349 JOURNAL COMPILATION ª 2009 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY 335 336 D. R. BELLWOOD ET AL. 2005). Indeed, they have been regularly identified as logical and behavioural variation. This includes at least indicator species of reef health (Reese, 1975; Roberts two different modes of coral feeding, exploitation of both et al., 1988; Kulbicki et al., 2005). It is this close associ- soft and hard corals, and a spectrum of coral feeding ation with corals and coral reefs that stands as one of the specializations ranging from highly specialized obligate most important features of this family. With almost a coral feeders that primarily target just one coral species to quarter of the species feeding on corals, they have what is facultative and generalist coral feeders that can feed on a arguably the closest association of any fish group with wide range of coral species (Pratchett et al., 2004; coral reefs. The key to understanding the history of this Berumen et al., 2005). relationship, however, is to obtain well-supported phy- The evolutionary history of these traits is poorly logenies based on multiple genes, and to use robust understood. Existing morphological and molecular phy- molecular dating methodologies, informed by reliable logenies have produced discordant tree topologies, open- fossil data, to provide a temporal framework in which to ing questions about the nature of character evolution. interpret recent ecological evidence. Most molecular analyses of the family have focused on Fossil evidence of increasing reef–fish interactions relationships between species pairs or species complexes points to a major change between the late Mesozoic (e.g. McMillan & Palumbi, 1995; Hsu et al., 2007) or have and the beginning of the Tertiary (Bellwood, 2003). included butterflyfishes as part of broader studies of Although there is a diverse range of acanthomorph fishes putative sister taxa (Bellwood et al., 2004). The most in the late Cretaceous, the earliest evidence of the vast comprehensive analysis to date using 3332 bp of mito- majority of extant reef fish families, for which there is a chondrial and nuclear DNA yielded a well-supported fossil record, is from the Eocene. Most of these families phylogeny, which differed significantly from all previous are first recorded from the 50-Myr-old deposits of Monte topologies, and underpinned a thorough evaluation of Bolca, in northern Italy (e.g. Blot, 1980; Bellwood, 1996; the systematics and taxonomy of the family (Fessler & although it should be noted that a few molecular studies Westneat, 2007). have suggested that some lineages may predate the The evolutionary and ecological ramifications of these Cretaceous ⁄ Tertiary (K ⁄ T) boundary, e.g. Streelman relationships for corallivory, however, have yet to be et al., 2002; Alfaro et al., 2007; Azuma et al., 2008). The fully explored. We address four critical questions: (1) Monte Bolca deposits mark the first modern coral reef How many times has corallivory arisen? (2) When did it fish assemblage in terms of both its taxonomic compo- first arise? (3) Did corallivory and ⁄ or a move onto coral sition and the functional attributes of the component reefs underpin diversification within the family? and (4) taxa (Bellwood, 1996), and it is here that we observe the What are the broader implications for the evolution of first evidence of increased interactions between fishes coral reefs? In this present study, we use a comprehen- and the benthos, with the appearance of several lineages sive new molecular phylogeny to explore the evolution- of fishes that were almost certainly grazing herbivores ary history of the family. For the first time, we use (Bellwood, 2003). Although there have been many molecular methods to examine the relationships between Eocene fossils ascribed to the Chaetodontidae, a recent all 10 genera and all respective subgenera (with the evaluation of this material has rejected all of these taxa; exception of Roa Roa sensu, Blum, 1988; = Roa, Kuiter, there is no reliable record of the family from the Eocene 2002). We examined 56 species using two nuclear (ETS2 (Bannikov, 2004). The oldest reliable fossil evidence for and S7I1) and a mitochondrial marker (cyt b); the nDNA the Chaetodontidae is of Miocene age (Carnevale, 2006). markers have not been used previously in this family. We However, with a robust molecular phylogeny we can also apply, for the first time, current Bayesian analyses build on the fossil record and place recent ecological for chronogram construction with multiple fossil calibra- advances in an evolutionary framework. tions. Using this chronogram, ecological evidence and Recent ecological research has provided a new per- diversification statistics, we explore the evolutionary spective on the nature of corallivory in reef fishes, origins of corallivory and the timing of this highly especially butterflyfishes. Building on existing informa- unusual fish–coral interaction. We then consider the tion (e.g. Birkeland & Neudecker, 1981; Blum, 1988; basis for these trophic innovations in the context of the Motta, 1988) recent studies have provided a detailed evolution of coral reefs. understanding of the family in terms of feeding mor- phology and kinematics (Ferry-Graham et al., 2001a,b; Materials and methods Konow et al., 2008; Konow & Ferry-Graham, in press), feeding strategies and behavioural interactions (Zekeria Taxon sampling et al., 2002; Gregson et al., 2008) and, most importantly, the nature and extent of corallivory (Pratchett et al., In total, 56 butterflyfish species were examined, with 2004; Berumen et al., 2005; Pratchett, 2005,