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.

Interactions between fishes and the benthos have shaped the development of marine ecosystems since at least the early Mesozoic. Here, using the morphology of fish teeth as an indicator of feeding abilities, we quantify changes over the last 240 million years of reef fish evolution. Fossil and extant coral reef fish assemblages reveal exceptional stasis in tooth design over time, with one notable exception, a distinct long-toothed form. Arising only in the last 40 million years, these long-toothed fishes have bypassed the invertebrate link in the food chain, feeding directly on benthic particulate material. With the appearance of elongated teeth, these specialized detritivores have moved from eating invertebrates to eating the food of invertebrates. Over evolutionary time, fishes have slid back down the food chain.

The evolution of ecological processes on coral reefs was examined based on Eocene fossil fishes from Monte Bolca, Italy and extant species from the Great Barrier Reef, Australia. Using ecologically relevant morphological metrics, we investigated the evolution of herbivory in surgeonfishes (Acanthuridae) and rabbitfishes (Siganidae). Eocene and Recent surgeonfishes showed remarkable similarities, with grazers, browsers and even specialized, long-snouted forms having Eocene analogues. These long-snouted Eocene species were probably pair-forming, crevice-feeding forms like their Recent counterparts. Although Eocene surgeonfishes likely played a critical role as herbivores during the origins of modern coral reefs, they lacked the novel morphologies seen in modern Acanthurus and Siganus (including eyes positioned high above their low-set mouths). Today, these forms dominate coral reefs in both abundance and species richness and are associated with feeding on shallow, exposed algal turfs. The radiation of these new forms, and their expansion into new habitats in the Oligocene–Miocene, reflects the second phase in the development of fish herbivory on coral reefs that is closely associated with the exploitation of highly productive short algal turfs.

Benthic crustaceans are an important component of the coral reef fauna, yet our understanding of their ecological significance is incomplete. To determine the community structure, abundance, biomass and productivity of benthic Crustacea at Lizard Island, a mid-shelf reef on the Great Barrier Reef, Australia, we investigated 5 major microhabitats: dead coral, coral rubble, sand, epilithic algal matrix (EAM) and fine-branching live coral. Crustacean communities differed significantly among habitats, with the exception of dead coral and coral rubble. Dead coral was the most important microhabitat type in terms of crustacean abundance (7838 ± 628 ind. 100 cm −2 , mean ± SE), biomass (0.75 ± 0.13 g m −2 , wet weight) and estimated productivity (0.17 ± 0.043 g 100 cm −2 yr −1 ash free dry weight). These values were 2 to 3 orders of magnitude greater than those for the least important habitats (EAM and fine-branching live coral). Despite their abundance, the average crustacean body length was just 0.79 ± 0.32 mm, largely due to the dominance of harpacticoid copepods. In contrast, decapods exhibited very low abundances, but yielded the greatest biomass and productivity and were particularly abundant in dead coral and coral rubble. The results highlight the importance of small crustaceans and dead coral microhabitats as valuable contributors to the trophic structure of coral reefs.

Key morphological traits reveal changes in functional morphospace occupation of reef fish assemblages over time. We used measurements of key functional attributes (i.e., lower jaw length and orbit diameter) of 208 fossil fish species from five geological periods to create bivariate plots of functional morphological traits through time. These plots were used to examine possible function and ecological characteristics of fossil reef fish assemblages throughout the Mesozoic and Cenozoic. A previously unknown trend of increasing orbit diameter over time became apparent. The Teleostei are the principal drivers of this change. The Eocene appears to mark a dramatic increase in two previously rare feeding modes in fishes: nocturnal feeding and high-precision benthic feeding. Interestingly, members of the Pycnodontiformes had relatively large eyes since the Triassic and appear to be the ecological precursors of their later teleost counterparts and may have been among the earliest nocturnal feeding fishes. Our results highlight potential changes in the roles of fishes on coral reefs through time.

The reef flat is one of the largest and most distinctive habitats on coral reefs, yet its role in reef trophodynamics is poorly understood. Evolutionary evidence suggests that reef flat colonization by grazing fishes was a major innovation that permitted the exploitation of new space and trophic resources. However, the reef flat is hydrodynamically challenging, subject to high predation risks and covered with sediments that inhibit feeding by grazers. To explore these opposing influences, we examine the Great Barrier Reef (GBR) as a model system. We focus on grazing herbivores that directly access algal primary productivity in the epilithic algal matrix (EAM). By assessing abundance, biomass, and potential fish productivity, we explore the potential of the reef flat to support key ecosystem processes and its ability to maintain fisheries yields. On the GBR, the reef flat is, by far, the most important habitat for turf‐grazing fishes, supporting an estimated 79% of individuals and 58% of the total biomass of grazing surgeonfishes, parrotfishes, and rabbitfishes. Approximately 59% of all (reef‐wide) turf algal productivity is removed by reef flat grazers. The flat also supports approximately 75% of all grazer biomass growth. Our results highlight the evolutionary and ecological benefits of occupying shallow‐water habitats (permitting a ninefold population increase). The acquisition of key locomotor and feeding traits has enabled fishes to access the trophic benefits of the reef flat, outweighing the costs imposed by water movement, predation, and sediments. Benthic assemblages on reefs in the future may increasingly resemble those seen on reef flats today, with low coral cover, limited topographic complexity, and extensive EAM. Reef flat grazing fishes may therefore play an increasingly important role in key ecosystem processes and in sustaining future fisheries yields.

No abstract

Jaw protrusion is one of the most important innovations in vertebrate feeding over the last 400 million years [1, 2]. Protrusion enables a fish to rapidly decrease the distance between itself and its prey [2, 3]. We assessed the evolution and functional implications of jaw protrusion in teleost fish assemblages from shallow coastal seas since the Cretaceous. By examining extant teleost fishes, we identified a robust morphological predictor of jaw protrusion that enabled us to predict the extent of jaw protrusion in fossil fishes. Our analyses revealed increases in both average and maximum jaw protrusion over the last 100 million years, with a progressive increase in the potential impact of fish predation on elusive prey. Over this period, the increase in jaw protrusion was initially driven by a taxonomic restructuring of fish assemblages, with an increase in the proportion of spiny-rayed fishes (Acanthomorpha), followed by an increase in the extent of protrusion within this clade. By increasing the ability of fishes to catch elusive prey [2, 4], jaw protrusion is likely to have fundamentally changed the nature of predator-prey interactions and may have contributed to the success of the spiny-rayed fishes, the dominant fish clade in modern oceans [5].