ELEVATED RATES OF MORPHOLOGICAL AND FUNCTIONAL DIVERSIFICATION IN REEF‐DWELLING HAEMULID FISHES

The relationship between habitat complexity and species richness is well established but comparatively little is known about the evolution of morphological diversity in complex habitats. Reefs are structurally complex, highly productive shallow‐water marine ecosystems found in tropical (coral reefs) and temperate zones (rocky reefs) that harbor exceptional levels of biodiversity. We investigated whether reef habitats promote the evolution of morphological diversity in the feeding and locomotion systems of grunts (Haemulidae), a group of predominantly nocturnal fishes that live on both temperate and tropical reefs. Using phylogenetic comparative methods and statistical analyses that take into account uncertainty in phylogeny and the evolutionary history of reef living, we demonstrate that rates of morphological evolution are faster in reef‐dwelling haemulids. The magnitude of this effect depends on the type of trait; on average, traits involved in the functional systems for prey capture and processing evolve twice as fast on reefs as locomotor traits. This result, along with the observation that haemulids do not exploit unique feeding niches on reefs, suggests that fine‐scale trophic niche partitioning and character displacement may be driving higher rates of morphological evolution. Whatever the cause, there is growing evidence that reef habitats stimulate morphological and functional diversification in teleost fishes.     

Do habitat shifts drive diversification in teleost fishes? An example from the pufferfishes (Tetraodontidae)

Habitat shifts are implicated as the cause of many vertebrate radiations, yet relatively few empirical studies quantify patterns of diversification following colonization of new habitats in fishes. The pufferfishes (family Tetraodon‐tidae) occur in several habitats, including coral reefs and freshwater, which are thought to provide ecological opportunity for adaptive radiation, and thus provide a unique system for testing the hypothesis that shifts to new habitats alter diversification rates. To test this hypothesis, we sequenced eight genes for 96 species of pufferfishes and closely related porcupine fishes, and added 19 species from sequences available in GenBank. We time‐calibrated the molecular phylogeny using three fossils, and performed several comparative analyses to test whether colonization of novel habitats led to shifts in the rate of speciation and body size evolution, central predictions of clades experiencing ecological adaptive radiation. Colonization of freshwater is associated with lower rates of cladogenesis in pufferfishes, although these lineages also exhibit accelerated rates of body size evolution. Increased rates of cladogenesis are associated with transitions to coral reefs, but reef lineages surprisingly exhibit significantly lower rates of body size evolution. These results suggest that ecological opportunity afforded by novel habitats may be limited for pufferfishes due to competition with other species, constraints relating to pufferfish life history and trophic ecology, and other factors.     

Speciation in coral-reef fishes

Covering <0·1% of the ocean’s surface, coral reefs harbour about one‐third of all marine fishes or c. 5000 species. Allopatry (geographic isolation) is believed to be the primary mode of speciation, yet few biogeographic barriers exist between reefs, and most reef fishes have a pelagic larval stage capable of extensive dispersal. Under these circumstances, why are there so many species of reef fishes? Since most biogeographic barriers in the oceans are either spatially or temporally permeable on a relatively short time frame, the requirement of isolation during allopatric speciation is hard to satisfy. Evidence from empirical and theoretical studies, the biological characteristics of coral reefs, and a reanalysis of biogeographic barriers indicate that sympatric speciation is possible but not common at small spatial scales and that parapatric speciation is a common (and probably the prevalent) mode of diversification in coral‐reef fishes. Regardless of the speciation mode, previous hypotheses of accelerated diversification in the Pleistocene due to sea level fluctuations are not supported by phylogenetic analyses. Recent developments in the area of comparative genomics can fuel a new revolution in the way marine speciation is studied.     

Influence of the geography of speciation on current patterns of coral reef fish biodiversity across the Indo‐Pacific

The role of speciation processes in shaping current biodiversity patterns represents a major scientific question for ecologists and biogeographers. Hence, numerous methods have been developed to determine the geography of speciation based on co‐occurrence between sister‐species. Most of these methods rely on the correlation between divergence time and several metrics based on the geographic ranges of sister‐taxa (i.e. overlap, asymmetry). The relationship between divergence time and these metrics has scarcely been examined in a spatial context beyond regression curves. Mapping this relationship across spatial grids, however, may unravel how speciation processes have shaped current biodiversity patterns through space and time. This can be particularly relevant for coral reef fishes of the Indo‐Pacific since the origin of the exceptional concentration of biodiversity in the Indo‐Australian Archipelago (IAA) has been actively debated, with several alternative hypotheses involving species diversification and dispersal. We reconstructed the phylogenetic relationships between three species‐rich families of coral reef fish (Chaetodontidae, Labridae, Pomacentridae) and calculated co‐occurrence metrics between closely related lineages of those families. We demonstrated that repeated biogeographic processes can be identified in present‐day species distribution by projecting co‐occurrence metrics between related lineages in a geographical context. Our study also evidence that sister‐species do not co‐occur randomly across the Indo‐Pacific, but tend to overlap their range within the IAA. We identified the imprint of two important biogeographic processes that caused this pattern in 48% of the sister‐taxa considered: speciation events within the IAA and repeated divergence between the Indian and Pacific Ocean, with subsequent secondary contact in the IAA.     

The biogeography of tropical reef fishes: endemism and provinciality through time

The largest marine biodiversity hotspot straddles the Indian and Pacific Oceans, driven by taxa associated with tropical coral reefs. Centred on the Indo‐Australian Archipelago (IAA), this biodiversity hotspot forms the ‘bullseye’ of a steep gradient in species richness from this centre to the periphery of the vast Indo‐Pacific region. Complex patterns of endemism, wide‐ranging species and assemblage differences have obscured our understanding of the genesis of this biodiversity pattern and its maintenance across two‐thirds of the world's oceans. But time‐calibrated molecular phylogenies coupled with ancestral biogeographic estimates have provided a valuable framework in which to examine the origins of coral reef fish biodiversity across the tropics. Herein, we examine phylogenetic and biogeographic data for coral reef fishes to highlight temporal patterns of marine endemism and tropical provinciality. The ages and distribution of endemic lineages have often been used to identify areas of species creation and demise in the marine tropics and discriminate among multiple hypotheses regarding the origins of biodiversity in the IAA. Despite a general under‐sampling of endemic fishes in phylogenetic studies, the majority of locations today contain a mixture of potential paleo‐ and neo‐endemic fishes, pointing to multiple historical processes involved in the origin and maintenance of the IAA biodiversity hotspot. Increased precision and sampling of geographic ranges for reef fishes has permitted the division of discrete realms, regions and provinces across the tropics. Yet, such metrics are only beginning to integrate phylogenetic relatedness and ancestral biogeography. Here, we integrate phylogenetic diversity with ancestral biogeographic estimation of lineages to show how assemblage structure and tropical provinciality has changed through time.     

The evolution of fishes and corals on reefs: form,function and interdependence

Coral reefs are renowned for their spectacular biodiversity and the close links between fishes and corals. Despite extensive fossil records and common biogeographic histories, the evolution of these two key groups has rarely been considered together. We therefore examine recent advances in molecular phylogenetics and palaeoecology, and place the evolution of fishes and corals in a functional context. In critically reviewing the available fossil and phylogenetic evidence, we reveal a marked congruence in the evolution of the two groups. Despite one group consisting of swimming vertebrates and the other colonial symbiotic invertebrates, fishes and corals have remarkably similar evolutionary histories. In the Paleocene and Eocene [66–34 million years ago (Ma)] most modern fish and coral families were present, and both were represented by a wide range of functional morphotypes. However, there is little evidence of diversification at this time. By contrast, in the Oligocene and Miocene (34–5.3 Ma), both groups exhibited rapid lineage diversification. There is also evidence of increasing reef area, occupation of new habitats, increasing coral cover, and potentially, increasing fish abundance. Functionally, the Oligocene–Miocene is marked by the appearance of new fish and coral taxa associated with high‐turnover fast‐growth ecosystems and the colonization of reef flats. It is in this period that the functional characteristics of modern coral reefs were established. Most species, however, only arose in the last 5.3 million years (Myr; Plio–Pleistocene), with the average age of fish species being 5.3 Myr, and corals just 1.9 Myr. While these species are genetically distinct, phenotypic differences are often limited to variation in colour or minor morphological features. This suggests that the rapid increase in biodiversity during the last 5.3 Myr was not matched by changes in ecosystem function. For reef fishes, colour appears to be central to recent diversification. However, the presence of pigment patterns in the Eocene suggests that colour may not have driven recent diversification. Furthermore, the lack of functional changes in fishes or corals over the last 5 Myr raises questions over the role and importance of biodiversity in shaping the future of coral reefs.     

Adaptive radiation in labrid fishes: A central role for functional innovations during 65 My of relentless diversification

Early burst patterns of diversification have become closely linked with concepts of adaptive radiation, reflecting interest in the role of ecological opportunity in modulating diversification. But, this model has not been widely explored on coral reefs, where biodiversity is exceptional, but many lineages have high dispersal capabilities and a pan‐tropical distribution. We analyze adaptive radiation in labrid fishes, arguably the most ecologically dominant and diverse radiation of fishes on coral reefs. We test for time‐dependent speciation, trophic diversification, and origination of 15 functional innovations, and early bursts in a series of functional morphological traits associated with feeding and locomotion. We find no evidence of time‐dependent or early burst evolution. Instead, the pace of speciation, ecological diversification, and trait evolution has been relatively constant. The origination of functional innovations has slowed over time, although few arose early. The labrid radiation seems to have occurred in response to extensive and still increasing ecological opportunity, but within a rich community of antagonists that may have prevented abrupt diversification. Labrid diversification is closely tied to a series of substantial functional innovations that individually broadened ecological diversity, ultimately allowing them to invade virtually every trophic niche held by fishes on coral reefs.     

Size-structural shifts reveal intensity of exploitation in coral reef fisheries

Fisheries exploitation represents a considerable threat to coral reef fish resources because even modest levels of extraction can alter ecological dynamics via shifts of stock size, species composition, and size-structure of the fish assemblage. Although species occupying higher trophic groups are known to suffer the majority of exploitative effects, changes in composition among lower trophic groups may be major, though are not frequently explored. Using size-based biomass spectrum analysis, we investigate the effects of fishing on the size-structure of coral reef fish assemblages spanning four geopolitical regions and determine if patterns of exploitation vary across trophic groups. Our analyses reveal striking evidence for the variety of effects fisheries exploitation can have on coral reef fish assemblages. When examining biomass spectra across the entire fish assemblage we found consistent evidence of size-specific exploitation, in which large-bodied individuals experience disproportionate reductions. The pattern was paralleled by and likely driven by, strongly size-specific reductions among top predators. In contrast, evidence of exploitation patterns was variable among lower trophic groups, in many cases including evidence of reductions across all size classes. The breadth of size classes and trophic groups that showed evidence of exploitation related positively to local human population density and diversity of fishing methods employed. Our findings highlight the complexity of coral reef fisheries and that the effects of exploitation on coral reefs can be realized throughout the entire fish assemblage, across multiple trophic groups and not solely restricted to large-bodied top-predators. Size-specific changes among fishes of lower trophic groups likely lead to altered ecological functioning of heavily exploited coral reefs. Together these findings reinforce the value of taking a multi-trophic group approach to monitoring and managing coral reef fisheries.     

Colour pattern as a single trait driving speciation in Hypoplectrus coral reef fishes?

Theory shows that speciation in the presence of gene flow occurs only under narrow conditions. One of the most favourable scenarios for speciation with gene flow is established when a single trait is both under disruptive natural selection and used to cue assortative mating. Here, we demonstrate the potential for a single trait, colour pattern, to drive incipient speciation in the genus Hypoplectrus (Serranidae), coral reef fishes known for their striking colour polymorphism. We provide data demonstrating that sympatric Hypoplectrus colour morphs mate assortatively and are genetically distinct. Furthermore, we identify ecological conditions conducive to disruptive selection on colour pattern by presenting behavioural evidence of aggressive mimicry, whereby predatory Hypoplectrus colour morphs mimic the colour patterns of non-predatory reef fish species to increase their success approaching and attacking prey. We propose that colour-based assortative mating, combined with disruptive selection on colour pattern, is driving speciation in Hypoplectrus coral reef fishes.     

Maintenance of fish diversity on disturbed coral reefs

Habitat perturbations play a major role in shaping community structure; however, the elements of disturbance-related habitat change that affect diversity are not always apparent. This study examined the effects of habitat disturbances on species richness of coral reef fish assemblages using annual surveys of habitat and 210 fish species from 10 reefs on the Great Barrier Reef (GBR). Over a period of 11 years, major disturbances, including localised outbreaks of crown-of-thorns sea star (Acanthaster planci), severe storms or coral bleaching, resulted in coral decline of 46–96% in all the 10 reefs. Despite declines in coral cover, structural complexity of the reef framework was retained on five and species richness of coral reef fishes maintained on nine of the disturbed reefs. Extensive loss of coral resulted in localised declines of highly specialised coral-dependent species, but this loss of diversity was more than compensated for by increases in the number of species that feed on the epilithic algal matrix (EAM). A unimodal relationship between areal coral cover and species richness indicated species richness was greatest at approximately 20% coral cover declining by 3–4 species (6–8% of average richness) at higher and lower coral cover. Results revealed that declines in coral cover on reefs may have limited short-term impact on the diversity of coral reef fishes, though there may be fundamental changes in the community structure of fishes.     

Latitudinal gradients in Atlantic reef fish communities: trophic structure and spatial use patterns

Trophic strategies and spatial use habits were investigated in reef fish communities. The results supported the hypothesis of differential use of food resources among tropical and higher latitude reef fishes, i.e . the number of species and relative abundance of fishes relying on relatively low‐quality food significantly decreased from tropical to temperate latitudes. The species : genus ratio of low‐quality food consumers increased toward the tropics, and was higher than the overall ratio considering all fishes in the assemblages. This supports the view that higher speciation rates occurred among this guild of fishes in warm waters. It was also demonstrated that density of herbivorous fishes (the dominant group relying on low‐quality food resources) in the western Atlantic decreased from tropical to temperate latitudes. Spatial use and mobility varied with latitude and consequently reef type and complexity. Fishes with small‐size home ranges predominated on tropical coral reefs.     

Community structure and biogeography of shore fishes in the Gulf of Aqaba,Red Sea

Shore fish community structure off the Jordanian Red Sea coast was determined on fringing coral reefs and in a seagrass-dominated bay at 6 m and 12 m depths. A total of 198 fish species belonging to 121 genera and 43 families was recorded. Labridae and Pomacentridae dominated the ichthyofauna in terms of species richness and Pomacentridae were most abundant. Neither diversity nor species richness was correlated to depth. The abundance of fishes was higher at the deep reef slope, due to schooling planktivorous fishes. At 12 m depth abundance of fishes at the seagrass-dominated site was higher than on the coral reefs. Multivariate analysis demonstrated a strong influence on the fish assemblages by depth and benthic habitat. Fish species richness was positively correlated with hard substrate cover and habitat diversity. Abundance of corallivores was positively linked with live hard coral cover. The assemblages of fishes were different on the shallow reef slope, deep reef slope and seagrass meadows. An analysis of the fish fauna showed that the Gulf of Aqaba harbours a higher species richness than previously reported. The comparison with fish communities on other reefs around the Arabian Peninsula and Indian Ocean supported the recognition of an Arabian subprovince within the Indian Ocean. The affinity of the Arabian Gulf ichthyofauna to the Red Sea is not clear. Received in revised form: 2 November 2001 Electronic Publication     

Widespread hybridization and bidirectional introgression in sympatric species of coral reef fish

Coral reefs are highly diverse ecosystems, where numerous closely related species often coexist. How new species arise and are maintained in these high geneflow environments have been long‐standing conundrums. Hybridization and patterns of introgression between sympatric species provide a unique insight into the mechanisms of speciation and the maintenance of species boundaries. In this study, we investigate the extent of hybridization between two closely related species of coral reef fish: the common coral trout (Plectropomus leopardus) and the bar‐cheek coral trout (Plectropomus maculatus). Using a complementary set of 25 microsatellite loci, we distinguish pure genotype classes from first‐ and later‐generation hybrids, identifying 124 interspecific hybrids from a collection of 2,991 coral trout sampled in inshore and mid‐shelf reefs of the southern Great Barrier Reef. Hybrids were ubiquitous among reefs, fertile and spanned multiple generations suggesting both ecological and evolutionary processes are acting to maintain species barriers. We elaborate on these finding to investigate the extent of genomic introgression and admixture from 2,271 SNP loci recovered from a ddRAD library of pure and hybrid individuals. An analysis of genomic clines on recovered loci indicates that 261 SNP loci deviate from a model of neutral introgression, of which 132 indicate a pattern of introgression consistent with selection favouring both hybrid and parental genotypes. Our findings indicate genome‐wide, bidirectional introgression between two sympatric species of coral reef fishes and provide further support to a growing body of evidence for the role of hybridization in the evolution of coral reef fishes.     

Repeated invasions into the twilight zone: evolutionary origins of a novel assemblage of fishes from deep Caribbean reefs

Mesophotic and deeper reefs of the tropics are poorly known and underexplored ecosystems worldwide. Collectively referred to as the ‘twilight zone’, depths below ~30–50 m are home to many species of reef fishes that are absent from shallower depths, including many undescribed and endemic species. We currently lack even a basic understanding of the diversity and evolutionary origins of fishes on tropical mesophotic reefs. Recent submersible collections in the Caribbean have provided new specimens that are enabling phylogenetic reconstructions that incorporate deep‐reef representatives of tropical fish genera. Here, we investigate evolutionary depth transitions in the family Gobiidae (gobies), the most diverse group of tropical marine fishes. Using divergence‐time estimation coupled with stochastic character mapping to infer the timing of shallow‐to‐deep habitat transitions in gobies, we demonstrate at least four transitions from shallow to mesophotic depths. Habitat transitions occurred in two broad time periods (Miocene, Pliocene–Pleistocene), and may have been linked to the availability of underutilized niches, as well as the evolution of morphological/behavioural adaptations for life on deep reefs. Further, our analysis shows that at least three evolutionary lineages that invaded deep habitats subsequently underwent speciation, reflecting another unique mode of radiation within the Gobiidae. Lastly, we synthesize depth distributions for 95 species of Caribbean gobies, which reveal major bathymetric faunal breaks at the boundary between euphotic and mesophotic reefs. Ultimately, our study is the first rigorous investigation into the origin of Caribbean deep‐reef fishes and provides a framework for future studies that utilize rare, deep‐reef specimens.     

Extinction vulnerability of coral reef fishes

With rapidly increasing rates of contemporary extinction, predicting extinction vulnerability and identifying how multiple stressors drive non-random species loss have become key challenges in ecology. These assessments are crucial for avoiding the loss of key functional groups that sustain ecosystem processes and services. We developed a novel predictive framework of species extinction vulnerability and applied it to coral reef fishes. Although relatively few coral reef fishes are at risk of global extinction from climate disturbances, a negative convex relationship between fish species locally vulnerable to climate change vs. fisheries exploitation indicates that the entire community is vulnerable on the many reefs where both stressors co-occur. Fishes involved in maintaining key ecosystem functions are more at risk from fishing than climate disturbances. This finding is encouraging as local and regional commitment to fisheries management action can maintain reef ecosystem functions pending progress towards the more complex global problem of stabilizing the climate.     

Geography and island geomorphology shape fish assemblage structure on isolated coral reef systems

We quantify the relative importance of multi‐scale drivers of reef fish assemblage structure on isolated coral reefs at the intersection of the Indian and Indo‐Pacific biogeographical provinces. Large (>30 cm), functionally‐important and commonly targeted species of fish, were surveyed on the outer reef crest/front at 38 coral reef sites spread across three oceanic coral reef systems (i.e. Christmas Island, Cocos (Keeling) Islands and the Rowley Shoals), in the tropical Indian Ocean (c. 1.126 x 106 km²). The effects of coral cover, exposure, fishing pressure, lagoon size and geographical context, on observed patterns of fish assemblage structure were modelled using Multivariate Regression Trees. Reef fish assemblages were clearly separated in space with geographical location explaining ~53 % of the observed variation. Lagoon size, within each isolated reef system was an equally effective proxy for explaining fish assemblage structure. Among local‐scale variables, ‘distance from port’, a proxy for the influence of fishing, explained 5.2% of total variation and separated the four most isolated reefs from Cocos (Keeling) Island, from reefs with closer boating access. Other factors were not significant. Major divisions in assemblage structure were driven by sister taxa that displayed little geographical overlap between reef systems and low abundances of several species on Christmas Island corresponding to small lagoon habitats. Exclusion of geographical context from the analysis resulted in local processes explaining 47.3% of the variation, highlighting the importance of controlling for spatial correlation to understand the drivers of fish assemblage structure. Our results suggest reef fish assemblage structure on remote coral reef systems in the tropical eastern Indian Ocean reflects a biogeographical legacy of isolation between Indian and Pacific fish faunas and geomorphological variation within the region, more than local fishing pressure or reef condition. Our findings re‐emphasise the importance that historical processes play in structuring contemporary biotic communities.     

A process‐based model supports an association between dispersal and the prevalence of species traits in tropical reef fish assemblages

Habitat dynamics interacting with species dispersal abilities could generate gradients in species diversity and prevalence of species traits when the latter are associated with species dispersal potential. Using a process‐based model of diversification constrained by a dispersal parameter, we simulated the interplay between reef habitat dynamics during the past 140 million years and dispersal, shaping lineage diversification history and assemblage composition globally. The emerging patterns from the simulations were compared to current prevalence of species traits related to dispersal for 6315 tropical reef fish species. We found a significant spatial congruence between the prevalence of simulated low dispersal values and areas with a large proportion of species characterized by small adult body size, narrow home range mobility behaviour, pelagic larval duration shorter than 21 days and diurnal activity. Species characterized by such traits were found predominantly in the Indo‐Australian Archipelago and the Caribbean Sea. Furthermore, the frequency distribution of the dispersal parameter was found to match empirical distributions for body size, PLD and home range mobility behaviour. Also, the dispersal parameter in the simulations was associated to diversification rates and resulted in trait frequency matching empirical distributions. Overall, our findings suggest that past habitat dynamics, in conjunction with dispersal processes, influenced diversification in tropical reef fishes, which may explain the present‐day geography of species traits.