Relationships of the temperate Australasian labrid fish tribe Odacini (Perciformes; Teleostei)

The labrid tribe Odacini comprises four genera and 12 species of fishes that inhabit shallow kelp forest and seagrass areas in temperate waters of Australia and New Zealand. Odacines are morphologically disparate, but share synapomorphies in fin structure and fusion of teeth into a beak-like oral jaw. A phylogenetic analysis of odacines was conducted to investigate their relationships to other labrid fishes, the relationships of species within the tribe, and the evolution of herbivory within the group. Fragments from two mitochondrial genes, 12S rDNA and 16S rDNA, and two nuclear genes, Tmo4C4 and RAG2, were sequenced for seven odacine species (representing all four genera), eight species representing the other major labrid lineages, and three outgroup species. Maximum likelihood and maximum parsimony analyses on the resulting 2338 bp of DNA sequence produced nearly identical topologies differing only in the placement of a clade containing the cheiline Cheilinus fasciatus and the scarine Cryptotomus roseus. The remaining clades received strong bootstrap support under maximum parsimony, and all clades in the maximum likelihood analysis received high bootstrap proportions and high posterior probabilities. The hypsigenyine labrid Choerodon anchorago formed the sister group to the odacines. Within the odacines, Odax cyanoallix+Odax pullus formed the sister to the remaining odacines, with Odax acroptilus, Odax cyanomelas, and Siphonognathus argyrophanes forming successively closer sister groups to the clade Haletta semifasciatus+Neoodax balteatus. Either herbivory evolved twice in the odacines, or herbivory evolved once with two reversions to carnivory. The latter hypothesis appears more likely in the light of odacine feeding biology.     

Phylogenetic relationships and the evolution of regulatory gene sequences in the parrotfishes

Regulatory genes control the expression of other genes and are key components of developmental processes such as segmentation and embryonic construction of the skull in vertebrates. Here we examine the variability and evolution of three vertebrate regulatory genes, addressing issues of their utility for phylogenetics and comparing the rates of genetic change seen in regulatory loci to the rates seen in other genes in the parrotfishes. The parrotfishes are a diverse group of colorful fishes from coral reefs and seagrasses worldwide and have been placed phylogenetically within the family Labridae. We tested phylogenetic hypotheses among the parrotfishes, with a focus on the genera Chlorurus and Scarus, by analyzing eight gene fragments for 42 parrotfishes and eight outgroup species. We sequenced mitochondrial 12s rRNA (967 bp), 16s rRNA (577 bp), and cytochrome b (477 bp). From the nuclear genome, we sequenced part of the protein-coding genes rag2 (715 bp), tmo4c4 (485 bp), and the developmental regulatory genes otx1 (672 bp), bmp4 (488bp), and dlx2 (522 bp). Bayesian, likelihood, and parsimony analyses of the resulting 4903 bp of DNA sequence produced similar topologies that confirm the monophyly of the scarines and provide a phylogeny at the species level for portions of the genera Scarus and Chlorurus. Four major clades of Scarus were recovered, with three distributed in the Indo-Pacific and one containing Caribbean/Atlantic taxa. Molecular rates suggest a Miocene origin of the parrotfishes (22 mya) and a recent divergence of species within Scarus and Chlorurus, within the past 5 million years. Developmentally important genes made a significant contribution to phylogenetic structure, and rates of genetic evolution were high in bmp4, similar to other coding nuclear genes, but low in otx1 and the dlx2 exons. Synonymous and non-synonymous substitution patterns in developmental regulatory genes support the hypothesis of stabilizing selection during the history of these genes, with several phylogenetic regions of accelerated non-synonymous change detected in the phylogeny.     

Phylogenetic relationships,evolution of broodcare behavior,and geographic speciation in the wrasse tribe Labrini

The family Labridae is a large assemblage of marine fish composed of about 580 species in 82 genera distributed in tropical and temperate marine waters around the world. Several subgroups, currently classified as tribes, have been identified in this large family, yet only a few phylogenetic analyses have been performed on labrid clades. We confirm monophyly of the labrid tribe Labrini and propose a phylogeny of the 23 species of the genera Acantholabrus, Centrolabras, Ctenolabrus, Labrus, Lappanella, Symphodus, Tautoga, and Tautogolabrus occurring in the eastern and western Atlantic and the Mediterranean. We analyzed a 577-bp segment of the mitochondrial 16S rDNA and a 506-bp segment of the mitochondrial control region in 22 species, for a total of up to 1069 bp per species. We used both parsimony and likelihood approaches under a variety of assumptions and models to generate phylogenetic hypotheses. The main features of the molecular phylogeny for the Labrini turned out to be the same for the two algorithms applied. The tree structure is similar to a previous, unpublished morphological phylogeny for a subset of labrine species. Estimated divergence times of the Labrini based on fossils and a molecular clock range from about 15 mya for the deepest splits to less than 1 mya for younger clades. Biogeographic patterns of the Symphodus species group and the genus Labrus are dominated by speciation events driven by the closing and opening of the Mediterranean Sea and periodic glaciation events during the past 1 million years. The Labrini are the only clade in the entire Labridae that exhibit nest-building and broodcare behavior. We use the phylogeny to show that similar broodcare behavior has evolved twice in the labrine fish and discuss scenarios for the evolution of broodcare from the diandric protogynous hermaphroditism found in ancestral labrines and many other wrasses.     

Local phylogenetic divergence and global evolutionary convergence of skull function in reef fishes of the family Labridae

The Labridae is one of the most structurally and functionally diversified fish families on coral and rocky reefs around the world, providing a compelling system for examination of evolutionary patterns of functional change. Labrid fishes have evolved a diverse array of skull forms for feeding on prey ranging from molluscs, crustaceans, plankton, detritus, algae, coral and other fishes. The species richness and diversity of feeding ecology in the Labridae make this group a marine analogue to the cichlid fishes. Despite the importance of labrids to coastal reef ecology, we lack evolutionary analysis of feeding biomechanics among labrids. Here, we combine a molecular phylogeny of the Labridae with the biomechanics of skull function to reveal a broad pattern of repeated convergence in labrid feeding systems. Mechanically fast jaw systems have evolved independently at least 14 times from ancestors with forceful jaws. A repeated phylogenetic pattern of functional divergence in local regions of the labrid tree produces an emergent family-wide pattern of global convergence in jaw function. Divergence of close relatives, convergence among higher clades and several unusual 'breakthroughs' in skull function characterize the evolution of functional complexity in one of the most diverse groups of reef fishes.     

A functional morphospace for the skull of labrid fishes: patterns of diversity in a complex biomechanical system

The Labridae (including wrasses, the Odacidae and the Scaridae) is a species‐rich group of perciform fishes whose members are prominent inhabitants of warm‐temperate and tropical reefs worldwide. We analyse functionally relevant morphometrics for the feeding apparatus of 130 labrid species found on the Great Barrier Reef and use these data to explore the morphological and mechanical basis of trophic diversity found in this assemblage. Morphological measurements were made that characterize the functional and mechanical properties of the oral jaws that are used in prey capture and handling, the hyoid apparatus that is used in expanding the buccal cavity during suction feeding, and the pharyngeal jaw apparatus that is used in breaking through the defences of shelled prey, winnowing edible matter from sand and other debris, and pulverizing the algae, detritus and rock mixture eaten by scarids (parrotfishes). A Principal Components Analysis on the correlation matrix of a reduced set of ten variables revealed complete separation of scarids from wrasses on the basis of the former having a small mouth with limited jaw protrusion, high mechanical advantage in jaw closing, and a small sternohyoideus muscle and high kinematic transmission in the hyoid four‐bar linkage. Some scarids also exhibit a novel four‐bar linkage conformation in the oral jaw apparatus. Within wrasses a striking lack of strong associations was found among the mechanical elements of the feeding apparatus. These weak associations resulted in a highly diverse system in which functional properties occur in many different combinations and reflect variation in feeding ecology. Among putatively monophyletic groups of labrids, the cheilines showed the highest functional diversity and scarids were moderately diverse, in spite of their reputation for being trophically monomorphic and specialized. We hypothesize that the functional and ecological diversity of labrids is due in part to a history of decoupled evolution of major components of the feeding system (i.e. oral jaws, hyoid and pharyngeal jaw apparatus) as well as among the muscular and skeletal elements of each component. © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 82 , 1–25.     

Molecular phylogeny and speciation of the surfperches (Embiotocidae, Perciformes).

Labroid fishes include a variety of families, such as wrasses (Labridae), odacids (Odacidae), damselfishes (Pomacentridae), parrotfishes (Scaridae), cichlids (Cichlidae), and surfperches (Embiotocidae). With only 23 species, the small embiotocid family exhibits a remarkably low species diversity compared to the large species diversity of the Cichlidae. Using mitochondrial DNA sequences of all 14 extant embiotocid genera, we established a molecular phylogeny of the family and compared it with a previously proposed morphological phylogeny. Genetic differentiation among embiotocids was compared to that among cichlids. Although species numbers are extremely different between these two families, the degrees of genetic differentiation within each family was found to be very similar.     

Distribution and abundance of labrids in northeastern New Zealand: the relationship between depth,exposure and pectoral fin aspect ratio

Physical factors influencing the distribution and abundance of seven common labrid fishes were examined over four rocky reef locations in northeastern New Zealand. Depth and exposure for each species (both within and among sexes) were related to pectoral fin aspect ratio. Each of the four locations (two mainland and two island) displayed distinct labrid assemblages, which were consistent over time, likely due to the influence of the East Auckland Current. There was a consistent depth-related trend for most species, regardless of location. Several species also showed a sex related depth difference. There was also a trend for some species to be associated with certain levels of wave exposure. For most species, the relationship between pectoral fin aspect ratio and the above physical variables was not as strongly evident in this temperate assemblage as has been previously found in tropical reef fish systems. Although some species did follow the predicted shifts in fin aspect ratio with depth and/or exposure, the observed trends were unrelated to fin aspect ratio for many other species. These findings suggest that wave exposure may not be as important for labrids on northeastern New Zealand reefs as it may be in tropical coral reefs systems. The lower fin aspect ratios for New Zealand labrids, compared to tropical labrids, suggest that New Zealand labrids represent a subset of the total pectoral fin diversity in the Labridae. Consequently, the potential for distinct trends in fin aspect ratio and physical variables to be evident may be reduced.     

Host preference and specialization in Gnathia sp., a common parasitic isopod of coral reef fishes

A gnathiid species (Crustacea: Isopoda; one of the most common ectoparasites of coral reef fishes) from the Great Barrier Reef, Australia, was allowed to choose among fishes from three different families to feed on (using two species of fishes per family). Gnathiids showed a strong preference for labrids, rarely feeding on pomacentrids or apogonids. In a separate experiment, gnathiid host preference did not vary among three labrid fish species. Gnathiids that fed on labrids had higher survival than those that fed on apogonids. Male gnathiids that fed on labrids also moulted to the adult stage more quickly. This suggests that host specialization and local adaptation might be occurring between these ectoparasites and their host fishes at the host fish family level.     

Does evolutionary innovation in pharyngeal jaws lead to rapid lineage diversification in labrid fishes?

Background  

Major modifications to the pharyngeal jaw apparatus are widely regarded as a recurring evolutionary key innovation that has enabled adaptive radiation in many species-rich clades of percomorph fishes. However one of the central predictions of this hypothesis, that the acquisition of a modified pharyngeal jaw apparatus will be positively correlated with explosive lineage diversification, has never been tested. We applied comparative methods to a new time-calibrated phylogeny of labrid fishes to test whether diversification rates shifted at two scales where major pharyngeal jaw innovations have evolved: across all of Labridae and within the subclade of parrotfishes.     

Global ecological success of Thalassoma fishes in extreme coral reef habitats

Phenotypic adaptations can allow organisms to relax abiotic selection and facilitate their ecological success in challenging habitats, yet we have relatively little data for the prevalence of this phenomenon at macroecological scales. Using data on the relative abundance of coral reef wrasses and parrotfishes (f. Labridae) spread across three ocean basins and the Red Sea, we reveal the consistent global dominance of extreme wave‐swept habitats by fishes in the genus Thalassoma, with abundances up to 15 times higher than any other labrid. A key locomotor modification—a winged pectoral fin that facilitates efficient underwater flight in high‐flow environments—is likely to have underpinned this global success, as numerical dominance by Thalassoma was contingent upon the presence of high‐intensity wave energy. The ecological success of the most abundant species also varied with species richness and the presence of congeneric competitors. While several fish taxa have independently evolved winged pectoral fins, Thalassoma appears to have combined efficient high‐speed swimming (to relax abiotic selection) with trophic versatility (to maximize exploitation of rich resources) to exploit and dominate extreme coral reef habitats around the world.     

Influence of sexual selection and feeding functional morphology on diversification rate of parrotfishes (Scaridae)

Scaridae (parrotfishes) is a prominent clade of 96 species that shape coral reef communities worldwide through their actions as grazing herbivores. Phylogenetically nested within Labridae, the profound ecological impact and high species richness of parrotfishes suggest that their diversification and ecological success may be linked. Here, we ask whether parrotfish evolution is characterized by a significant burst of lineage diversification and whether parrotfish diversity is shaped more strongly by sexual selection or modifications of the feeding mechanism. We first examined scarid diversification within the greater context of labrid diversity. We used a supermatrix approach for 252 species to propose the most extensive phylogenetic hypothesis of Labridae to date, and time-calibrated the phylogeny with fossil and biogeographical data. Using divergence date estimates, we find that several parrotfish clades exhibit the highest diversification rates among all labrid lineages. Furthermore, we pinpoint a rate shift at the shared ancestor of Scarus and Chlorurus, a scarid subclade characterized by territorial behaviour and strong sexual dichromatism, suggesting that sexual selection was a major factor in parrotfish diversification. Modifications of the pharyngeal and oral jaws that happened earlier in parrotfish evolution may have contributed to this diversity by establishing parrotfishes as uniquely capable reef herbivores.     

Ecomorphology: Experimental Functional Anatomy for Ecological Problems

It is generally believed that the functional design of an organismrelates to its ecology, yet this ecomorphological paradigm hashistorically suffered from the lack of a rigorous frameworkfor its implementation. I present a methodology for experimentallyexploring the ecological consequences of variation in morphology.The central idea is that morphology influences ecology by limitingthe ability of the individual to perform key tasks in its dailylife. Inthis scheme the effect of morphological variation onbehavioral performance is first tested in laboratory experiments.As the behavioral capability of an individual defines the rangeof ecological resources that it can potentially make use of(the potential niche), the second step in the scheme involvescomparing the potential niche of an individual to actual patternsof resource use (the realized niche). This permits a quantitativeassessment of the significance of an organism's maximal capabilitiesin determining actual patterns of resource use. An example is presented from work on the feeding biology offishes in the family Labridae (wrasses and parrotfishes). Mostlabrids feed by crushing shelled prey in their powerful pharyngealjaws. This example explores the dietary consequences of variationin crushing strength amongand within species. Crushing strengthwas estimated from biomechanical analyses of the crushingapparatusin several species, and these predictions of relative strengthwere tested in laboratory feeding experiments with hard-shelledprey. Morphology accurately predicted relative crushing ability,and the final section of the study explored the effect of variationin crushing ability on diet. Within each of three species crushingstrength appears to underlie a major ontogentic dietary switchfrom soft-bodied prey to a diet dominated by hard-shelled prey.In each species this switch occurred at about the same crushingstrength, around 5 Newtons (N), in spite of the fact that thiscrushing strength is achieved by the three species at differentbody sizes. Diet breadth increases during ontogeny in each species,until a crushing strength of 5 N is achieved, when diet breadthbegins to decline. The strongest fishes specialized almost entirelyon molluscs and sea urchins. Thus, these labrids take advantageof ontogenetic and interspecific differences in crushing strengthby including harder and harder prey in their diet, and ultimatelyspecializing on hard prey types. The specialized organizationof the labrid pharyngeal jaws can be viewed as a key innovationthat has permitted this lineage of fishes to invade the mollusceating niche, a relatively empty trophic niche within the highlyspeciose and diverse communities of coral reef fishes.     

Ancient origins of Indo-Pacific coral reef fish biodiversity: a case study of the leopard wrasses (Labridae: Macropharyngodon)

Temporal origins of reef fishes in the Indo-Australian Archipelago were examined using wrasses in the genus Macropharyngodon. The genus was selected as it is morphologically and ecologically distinct, with strongly reef-associated species exhibiting discrete distributions across the Indo-Pacific. Phylogenetic relationships were explored using COI, 16S, and 12S rRNA mitochondrial sequences. Monophyly of the genus was supported by congruent Bayesian, maximum likelihood, and maximum parsimony trees. Estimates of lineage ages based on fossil-calibrated reef fish divergences suggest that Macropharyngodon had an extensive evolutionary history starting in the early Miocene. Repeated divergences of Indian Ocean-Pacific Ocean lineages appear to have occurred over at least 19 million years. Regional endemics represent both old and young clades. Our estimates of early Miocene origins, and mid-Miocene to Pliocene diversifications of Macropharyngodon are supported by recent studies of other reef fish genera, and emphasise the importance of pre-Pleistocene events in generating Indo-Pacific coral reef fish biodiversity.     

Impacts of predator depletion by fishing on the biomass and diversity of non-target reef fish communities

 An understanding of the indirect effects of fishing on predator-prey relationships is required for the development of valid multispecies yield models for reef fisheries and for determining the factors governing fish community structure at larger scales. We used an underwater visual census technique to examine the indirect effects of fishing on the biomass and diversity (species richness) of reef fishes in a series of ten traditional Fijian fishing grounds (qoliqoli) subject to a range of fishing intensities. All members of the families Chaetodontidae (butterflyfishes), Labridae (wrasses), Lutjanidae (snappers), Mullidae (goatfishes), Scaridae (parrotfishes) and the sub-family Epinephelinae (groupers and coral trout) which could be reliably identified were censused. Each species censused was assigned to one of three trophic groups: herbivore, invertebrate feeder or piscivore. The biomass of all piscivorous fishes and of large (>30 cm) piscivorous fishes differed significantly between qoliqoli and was significantly correlated with fishing intensity. However, the biomass of piscivorous fishes was not correlated with the biomass or diversity of their potential prey (which were not targeted by the fishery). This suggested that the indirect effects of fishing did not have an important bearing on fish diversity or biomass and that predation by the target species did not play an important role in structuring these Fijian reef fish communities. The results contrast with those from a number of studies at smaller scales and provided further indications that the structure of reef fish communities is not governed by a single dominant process, but by a range of processes which operate on different scales in different circumstances. Accepted: 29 July 1996     

Locomotion in labrid fishes: implications for habitat use and cross-shelf biogeography on the Great Barrier Reef

Coral reefs exhibit marked zonation patterns within single reefs and across continental shelves. For sessile organisms these zones are often related to wave exposure. We examined the extent to which wave exposure may shape the distribution patterns of fishes. We documented the distribution of 98 species of wrasses and parrotfishes at 33 sites across the Great Barrier Reef. The greatest difference between labrid assemblages was at the habitat level, with exposed reef flats and crests on mid- and outer reefs possessing a distinct faunal assemblage. These exposed sites were dominated by individuals with high pectoral fin aspect ratios, i.e. fishes believed to be capable of lift-based swimming which often achieve high speeds. Overall, there was a strong correlation between estimated swimming performance, as indicated by fin aspect ratio, and degree of water movement. We propose that swimming performance in fishes limits access to high-energy locations and may be a significant factor influencing habitat use and regional biogeography of reef fishes.     

A molecular phylogeny and classification of Bignoniaceae

Bignoniaceae are woody, trees, shrubs, and lianas found in all tropical floras of the world with lesser representation in temperate regions. Phylogenetic analyses of chloroplast sequences (rbcL, ndhF, trnL-F) were undertaken to infer evolutionary relationships in Bignoniaceae and to revise its classification. Eight clades are recognized as tribes (Bignonieae, Catalpeae, Coleeae, Crescentieae, Jacarandeae, Oroxyleae, Tecomeae, Tourrettieae); additional inclusive clades are named informally. Jacarandeae and Catalpeae are resurrected; the former is sister to the rest of the family, and the latter occupies an unresolved position within the "core" Bignoniaceae. Tribe Eccremocarpeae is included in Tourrettieae. Past classifications recognized a large Tecomeae, but this tribe is paraphyletic with respect to all other tribes. Here Tecomeae are reduced to a clade of approximately 12 genera with a worldwide distribution in both temperate and tropical ecosystems. Two large clades, Bignonieae and Crescentiina, account for over 80% of the species in the family. Coleeae and Crescentieae are each included in larger clades, the Paleotropical alliance and Tabebuia alliance, respectively; each alliance includes a grade of taxa assigned to the traditional Tecomeae. Parsimony inference suggests that the family originated in the neotropics, with at least five dispersal events leading to the Old World representatives.     

Molecular phylogeny of deer (Cervidae: Artiodactyla)

Sequences of mitochondrial genes 12S and 16S rRNA (2 445 bp) and the region of the nuclear beta-spectrin gene (828 bp) were analyzed in members of the family Cervidae and in other artiodactyls. Several molecular synapomorphies characteristic both of Cervidae and musk deer have been found. According to our data, Cervidae is a sister clade to Bovidae, which are very close to Moschidae. The family Giraffidae is exterior to this common clade, while Antilocapridae occupies a more basal position. The family Cervidae proper splits into three clades including the genera Cervus and Muntiacus (1), Capreolus, Hydropotes, Alces (2), and Rangifer, Odocoileus, and the remaining genera (3). In general, our phylogenetic reconstructions conform to the results of earlier molecular genetic studies, but substantially differ from the traditional taxonomy of Ruminantia.     

Chemical and physical defenses of Singapore gorgonians (Octocorallia: Gorgonacea)

Gorgonians are abundant in tropical waters and their polyps are seldom predated on. This study investigates how gorgonians defend themselves chemically and physically against fish predation. Gorgonian extracts and sclerites were incorporated into fish feed and tested on reef fishes. Laboratory bioassays using Greyhead wrasses, Halichoeres purpurescens, as well as field bioassays showed five gorgonian species from the family Ellisellidae and three from the family Plexauridae collected from Singapore reefs to be deterrent towards fishes. Bioassays of fractions obtained from subsequent fractionation suggested synergistic or additive effects between compounds present in gorgonians. Sclerites incorporated into fish feed in their natural concentrations were also tested for fish deterrence and were positive for only two gorgonian species from the family Ellisellidae.     

Non‐reef habitats in a tropical seascape affect density and biomass of fishes on coral reefs

Nonreef habitats such as mangroves, seagrass, and macroalgal beds are important for foraging, spawning, and as nursery habitat for some coral reef fishes. The spatial configuration of nonreef habitats adjacent to coral reefs can therefore have a substantial influence on the distribution and composition of reef fish. We investigate how different habitats in a tropical seascape in the Philippines influence the presence, density, and biomass of coral reef fishes to understand the relative importance of different habitats across various spatial scales. A detailed seascape map generated from satellite imagery was combined with field surveys of fish and benthic habitat on coral reefs. We then compared the relative importance of local reef (within coral reef) and adjacent habitat (habitats in the surrounding seascape) variables for coral reef fishes. Overall, adjacent habitat variables were as important as local reef variables in explaining reef fish density and biomass, despite being fewer in number in final models. For adult and juvenile wrasses (Labridae), and juveniles of some parrotfish taxa (Chlorurus), adjacent habitat was more important in explaining fish density and biomass. Notably, wrasses were positively influenced by the amount of sand and macroalgae in the adjacent seascape. Adjacent habitat metrics with the highest relative importance were sand (positive), macroalgae (positive), and mangrove habitats (negative), and fish responses to these metrics were consistent across fish groups evaluated. The 500‐m spatial scale was selected most often in models for seascape variables. Local coral reef variables with the greatest importance were percent cover of live coral (positive), sand (negative), and macroalgae (mixed). Incorporating spatial metrics that describe the surrounding seascape will capture more holistic patterns of fish–habitat relationships on reefs. This is important in regions where protection of reef fish habitat is an integral part of fisheries management but where protection of nonreef habitats is often overlooked.