Patterns and Processes in the Evolutionary History of Parrotfishes
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bs_bs_banner Biological Journal of the Linnean Society, 2012, ••, ••–••. With 5 figures Patterns and processes in the evolutionary history of parrotfishes (Family Labridae) JOHN. H. CHOAT1*, OYA. S. KLANTEN1†, LYNNE VAN HERWERDEN1, D. ROSS ROBERTSON2‡ and KENDALL D. CLEMENTS3 1School of Tropical and Marine Biology, James Cook University, Townsville, QLD, 4811, Australia 2Smithsonian Tropical Research Institute, Ancon, Balboa, Republic of Panama 3School of Biological Sciences, University of Auckland, Private Bag 92019, Auckland 1142, New Zealand Received 5 March 2012; revised 23 May 2012; accepted for publication 23 May 2012 Phylogenetic reconstruction of the evolutionary relationships among 61 of the 70 species of the parrotfish genera Chlorurus and Scarus (Family Labridae) based on mitochondrial and nuclear gene sequences retrieved 15 well-supported clades with mid Pliocene/Pleistocene diversification. Twenty-two reciprocally monophyletic sister- species pairs were identified: 64% were allopatric, and the remainder were sympatric. Age of divergence was similar for allopatric and sympatric species pairs. Sympatric sister pairs displayed greater divergence in morphol- ogy, ecology, and sexually dimorphic colour patterns than did allopatric pairs, suggesting that both genetic drift in allopatric species pairs and ecologically adaptive divergence between members of sympatric pairs have played a role in diversification. Basal species typically have small geographical ranges and are restricted to geographically and ecologically peripheral reef habitats. We found little evidence that a single dominant process has driven diversification, nor did we detect a pattern of discrete, sequential stages of diversification in relation to habitat, ecology, and reproductive biology. The evolution of Chlorurus and Scarus has been complex, involving a number of speciation processes. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ••, ••–••. ADDITIONAL KEYWORDS: adaptive radiation – evolution – sexual selection – speciation – reef fish. INTRODUCTION tionary trajectories, diverging sequentially along axes of habitat, trophic morphology, and communication Adaptive radiations are episodes of phenotypic diver- (Streelman & Danley, 2003). Under this model, the sification in rapidly multiplying lineages that result first two stages (ecological) are driven by natural in ecologically divergent groups of species (Schluter, selection, and the third (reproductive) is driven by 2000). A pervasive theme in the vertebrate literature sexual selection (Streelman & Danley, 2003). One of concerns the concept of radiation as a series of stages, the primary exemplars for this model of adaptive in which diversification proceeds through discrete radiation was the evolution of parrotfishes, compris- sequences of phenotypic differentiation (Streelman ing a speciose group of fishes confined largely to coral et al., 2002; Streelman & Danley, 2003; Sallan & reefs (Streelman et al., 2002; Streelman & Danley, Friedman, 2012). The most relevant example in this 2003). As a result, the processes of sequential diver- context is the model of radiation by stages in which sification under this radiation in stages model have different vertebrate radiations follow similar evolu- been applied to the evolution of reef fish faunas, especially the Labridae (Smith et al., 2008; Kazanci- og˘lu et al., 2009). However, recent studies suggest *Corresponding author. E-mail: [email protected] that aspects of this model require reconsideration. †Current address: School of Medicine, The University of Sydney, Building F13, Sydney, NSW 2006, Australia First, the concept of sequential action of natural and ‡Mailing address: STRI, Unit 0948, APO AA 34002, USA sexual selection could be profitably re-examined to © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ••, ••–•• 1 2 J. H. CHOAT ET AL. determine whether these processes are contempora- The evidence for a recent and rapid diversification in neous and interacting, rather than separate in scarines (Alfaro et al., 2009; Kazanciog˘lu et al., 2009), time (The Marie Curie Speciation Network*, 2012). coupled with the analysis of morphological evolution of Second, explicit tests have questioned the concept of the pharyngeal and oral jaws (Price et al., 2010), has radiation in stages (Sallan & Friedman, 2012). Third, focused attention on the processes underlying their the extent to which alternative evolutionary processes speciation. Initial studies (Streelman et al., 2002) iden- such as neutral divergence after geographical isola- tified a pattern of diversification that represented a tion have been important in the evolution of parrot- classical example of an adaptive radiation, with a fishes requires further examination (Robertson et al., signature of natural and sexual selection (Streelman & 2006). The main aim of the present study was to Danley, 2003). These studies suggested that partition- examine the pattern of species-level divergences in ing by habitat occurred in the deepest evolutionary the most speciose clades of parrotfishes aiming to nodes, with sparisomatinine (primarily Sparisoma and determine the extent to which they conform to a Calotomus) species being associated with seagrass model of adaptive radiation as an explanation for the habitats, and scarinines (Bolbometopon, Cetoscarus, diversity of this group. Hipposcarus, Chlorurus, and Scarus) associated with The parrotfishes are a clade of speciose (ten genera, coral reefs. Trophic diversification was visualized in 99 recognized species; Parenti & Randall, (2011) terms of the development of scraping or excavating but morphologically uniform (Bellwood, 1994) perci- feeding modes linked to the fusion of dental plates and form fishes notable both for their abundance on jaw articulations that provided flexibility (for scraping) present day tropical reef systems and their pre- and increased power (for excavating) calcareous reef sumed functional importance (Bellwood & Wain- substrata. Streelman & Danley (2003) further pro- wright, 2002).They were previously recognized as a posed that the dominant element in the more recent distinct family, the Scaridae, closely related to the diversification of lineages within the scarine clade Labridae and comprising two sub-familial groups: the involved socio-sexual behaviour (male territoriality scarines and sparisomatines. Phylogenetic analysis and breeding systems), and associated colour pattern (Westneat & Alfaro, 2005) revealed that the parrot- development, with sexual selection the primary fishes are nested within a monophyletic Labridae and process. are sister to cheiline labrids. Parrotfishes (scarinae) Subsequent studies (Alfaro et al., 2009; Kazanci- are therefore referred to as scarine labrids in the og˘lu et al., 2009; Price et al., 2010) analyzed rates of present study. morphological change in the scarine labrids and the The most speciose elements of this taxon, the extent to which modification of the pharyngeal and genera Scarus, Chlorurus, and Sparisoma, display a oral jaws may be implicated in the diversification of pattern of recent diversification that is restricted speciose clades of parrotfishes. These studies con- largely to the last 3.5 million years (Robertson et al., cluded that that, although changes in the pharyngeal 2006; Smith et al., 2008; Alfaro et al., 2009). The (Alfaro et al., 2009) and especially the oral jaws (Price distribution of diversity is uneven in terms of taxo- et al., 2010) of scarinine parrotfishes occurred at a nomic structure and biogeography. A single genus, greater rate than observed in other labrid taxa, and, Scarus, accounts for over 50% of the species, and 70% in the latter case, were correlated with lineage diver- of all known scarines occur in the Tropical East sification, these changes were not the underlying Pacific and Indo-West Pacific biogeographical regions cause of the cladogenesis that characterizes some (Parenti & Randall, 2000, 2011). Parrotfish are rela- groups of parrotfishes. Alfaro et al. (2009) and Kazan- tively uniform in terms of morphology and foraging ciog˘lu et al. (2009) concluded that the pattern of modes, usually grazing in multi-specific schools over increased rates of diversification was better explained rock and calcareous substrata, (Bellwood & Choat, by the evolution of extreme dichromatism (and other 1990; Bellwood, 1994). This morphological uniformity social and behavioural characters relating to sexual contrasts with the complex reproductive biology of selection) within Scarus and Chlorurus. This conclu- parrotfishes; most are protogynous hermaphrodites, sion was consistent with the sequential pattern of with many taxa manifesting distinctive sexually diversification proposed by Streelman & Danley dimorphic colour patterns (Choat & Robertson, 1975; (2003). Robertson & Warner, 1978; Kazanciog˘lu & Alonzo, Previous phylogenetic analyses (approximately 2010) and plasticity in somatic growth (Gust, 2004; 50% of the known species of Chlorurus and Scarus) Munday et al., 2004). This combination of taxonomic, focussed on the roles of ecological diversification and ecological, and reproductive characteristics has sexual selection as factors driving diversification. The prompted a number of studies on their evolutionary role of geographical isolation as a process driving history, with nine phylogenetic analyses emerging diversification has not been considered in detail. over the last decade. Identification of sister taxa, analysis of geographical