The disparity in species richness among evolutionary lineages is one of the oldest and most intriguing issues in evolutionary biology. Although geographical factors have been traditionally thought to promote speciation, recent studies have underscored the importance of ecological interactions as one of the main drivers of diversification. Here, we test if differences in species richness of closely related lineages match predictions based on the concept of density-dependent diversification. As radiation progresses, ecological niche-space would become increasingly saturated, resulting in fewer opportunities for speciation. To assess this hypothesis, we tested whether reef fish niche shifts toward usage of low-quality food resources (i.e. relatively low energy/protein per unit mass), such as algae, detritus, sponges and corals are accompanied by rapid net diversification. Using available molecular information, we reconstructed phylogenies of four major reef fish clades (Acanthuroidei, Chaetodontidae, Labridae and Pomacentridae) to estimate the timing of radiations of their subclades. We found that the evolution of species-rich clades was associated with a switch to low quality food in three of the four clades analyzed, which is consistent with a density-dependent model of diversification. We suggest that ecological opportunity may play an important role in understanding the diversification of reef-fish lineages.
Reef fishes are an exceptionally speciose vertebrate assemblage, yet the main drivers of their diversification remain unclear. It has been suggested that Miocene reef rearrangements promoted opportunities for lineage diversification, however, the specific mechanisms are not well understood. Here, we assemble near-complete reef fish phylogenies to assess the importance of ecological and geographical factors in explaining lineage origination patterns. We reveal that reef fish diversification is strongly associated with species' trophic identity and body size. Large-bodied herbivorous fishes outpace all other trophic groups in recent diversification rates, a pattern that is consistent through time. Additionally, we show that omnivory acts as an intermediate evolutionary step between higher and lower trophic levels, while planktivory represents a common transition destination. Overall, these results suggest that Miocene changes in reef configurations were likely driven by, and subsequently promoted, trophic innovations. This highlights trophic evolution as a key element in enhancing reef fish diversification.
Herbivory by fishes has been identified as a key ecological process shaping coral reefs through time. Although taxonomically limited, herbivorous reef fishes display a wide range of traits, which results in varied ecosystem functions on reefs around the world. Yet, we understand little about how these trait combinations and functions in ecosystems changed through time and across biogeographic realms. Here, we used fossils and phylogenies in a functional ecological framework to reveal temporal changes in nominally herbivorous fish assemblages among oceanic basins in both trait space and lineage richness among functions. We show that the trait space occupied by extant herbivorous fishes in the Indo-Pacific resulted from an expansion of traits from the ancestral Tethyan assemblages. By contrast, trait space in the Atlantic is the result of lineage turnover, with relatively recent colonization by lineages that arose in the east Tethys/Indo-Pacific. From an ecosystem function perspective, the Atlantic supports a depauperate fauna, with few extant herbivorous reef fish lineages performing each function. Indo-Pacific fishes support both more functions and more lineages within each function, with a marked Miocene to Pleistocene expansion. These disparities highlight the importance of history in explaining global variation in fish functional composition on coral reefs.
The charismatic trumpetfishes, goatfishes, dragonets, flying gurnards, seahorses, and pipefishes encompass a recently defined yet extraordinarily diverse clade of percomorph fishes—the series Syngnatharia. This group is widely distributed in tropical and warm-temperate regions, with a great proportion of its extant diversity occurring in the Indo-Pacific. Because most syngnatharians feature long-range dispersal capabilities, tracing their biogeographic origins is challenging. Here, we applied an integrative phylogenomic approach to elucidate the evolutionary biogeography of syngnatharians. We built upon a recently published phylogenomic study that examined ultraconserved elements by adding 62 species (total 169 species) and one family (Draconettidae), to cover ca. 25% of the species diversity and all 10 families in the group. We inferred a set of time-calibrated trees and conducted ancestral range estimations. We also examined the sensitivity of these analyses to phylogenetic uncertainty (estimated from multiple genomic subsets), area delimitation, and biogeographic models that include or exclude the jump-dispersal parameter (j). Of the three factors examined, we found that the j parameter has the strongest effect in ancestral range estimates, followed by number of areas defined, and tree topology and divergence times. After accounting for these uncertainties, our results reveal that syngnatharians originated in the ancient Tethys Sea ca. 87 Ma (84–94 Ma; Late Cretaceous) and subsequently occupied the Indo-Pacific. Throughout syngnatharian history, multiple independent lineages colonized the eastern Pacific (6–8 times) and the Atlantic (6–14 times) from their center of origin, with most events taking place following an east-to-west route prior to the closure of the Tethys Seaway ca. 12–18 Ma. Ultimately, our study highlights the importance of accounting for different factors generating uncertainty in macroevolutionary and biogeographic inferences.
Functional traits have been fundamental to the evolution and diversification of entire fish lineages on coral reefs. Yet their relationship with the processes promoting speciation, extinction and the filtering of local species pools remains unclear. We review the current literature exploring the evolution of diet, body size, water column use and geographic range size in reef-associated fishes. Using published and new data, we mapped functional traits on to published phylogenetic trees to uncover evolutionary patterns that have led to the current functional diversity of fishes on coral reefs. When examining reconstructed patterns for diet and feeding mode, we found examples of independent transitions to planktivory across different reef fish families. Such transitions and associated morphological alterations may represent cases in which ecological opportunity for the exploitation of different resources drives speciation and adaptation. In terms of body size, reconstructions showed that both large and small sizes appear multiple times within clades of mid-sized fishes and that extreme body sizes have arisen mostly in the last 10 million years (Myr). The reconstruction of range size revealed many cases of disparate range sizes among sister species. Such range size disparity highlights potential vicariant processes through isolation in peripheral locations. When accounting for peripheral speciation processes in sister pairs, we found a significant relationship between labrid range size and lineage age. The diversity and evolution of traits within lineages is influenced by trait-environment interactions as well as by species and trait-trait interactions, where the presence of a given trait may trigger the development of related traits or behaviours. Our effort to assess the evolution of functional diversity across reef fish clades adds to the burgeoning research focusing on the evolutionary and ecological roles of functional traits. We argue that the combination of a phylogenetic and a functional approach will improve the understanding of the mechanisms of species assembly in extraordinarily rich coral reef communities.
Aim To examine the dynamics among the processes of speciation, extinction and dispersal in marine environments using phylogenies to reveal the evolutionary mechanisms that promote latitudinal differences in biodiversity. Using phylogenetic comparative methods we assess whether tropical reef fish lineages show higher diversification rates and whether the majority of extratropical reef fish lineages have originated from tropical areas. Location Shallow water tropical and extratropical reefs globally. Methods Using fossil‐calibrated phylogenies for four reef‐associated fish families (Chaetodontidae, Labridae, Pomacentridae and Sparidae) we apply evolutionary models (GeoSSE and HiSSE) that allow the estimation of speciation, extinction and dispersal rates associated with geographical ranges and explore potential biases from unsampled characters. Results We found that tropical lineages show higher rates of speciation and tended to have lower extinction rates. Overall, we identify higher net diversification rates for tropical lineages compared with those in extratropical regions in all four families. Rates of dispersal tended to be higher for lineages with tropical origins expanding into extratropical regions. Within the family Labridae, two tropical lineages were found to exhibit higher net diversification rates, above that expected from latitudinal differences. Main conclusions Our results offer support for the predictions of the ‘out of the tropics’ and ‘evolutionary speed’ models of evolution, both of which highlight the marine tropics as an important evolutionary engine promoting latitudinal differences in reef fish biodiversity. Moreover, we find that two tropical labrid lineages are undergoing exceptional diversification associated with additional traits, possibly linked with the extreme sexual dichromatism observed in both clades.
Aim To describe the global biogeography of key herbivorous coral reef fish groups since their presumed origins, using data from both fossil and extant species. Location Global Cenozoic reefs. Taxon Acanthuridae (surgeonfishes), Siganidae (rabbitfishes) and Scarini (parrotfishes). Methods We applied the fossilized birth–death model to build chronograms including a comprehensive sampling of extant species and all the fossil occurrences described for each group. With the resulting chronograms, we built biogeographical models considering the geological changes in reef habitat availability since the ancient Tethys Sea. Finally, we used biogeographical stochastic mappings to trace the routes of colonization of the Atlantic Ocean by lineages in our focal taxa. Results We found that the Palaeocene–Eocene was a period of significant lineage origination for surgeonfishes and rabbitfishes in the central Tethys Sea with the appearance of ancient genera. Most of these genera were probably extinct by the Eocene–Oligocene boundary as they do not correspond with modern taxa. Parrotfishes, however, originated in the early Oligocene, an epoch that corresponds with the geographical transition of the marine biodiversity hotspot. In all groups, extant genera had similar origin times and all expanded in the Miocene, mainly in the Indo‐Pacific. In the Atlantic, only one parrotfish lineage with Tethyan ancestry appears to have survived. It subsequently gave rise to extant endemic genera (Sparisoma and Cryptotomus). The other extant lineages in the Atlantic all have Indo‐Pacific origins and colonized more recently using different dispersal pathways. Main conclusions The Indo‐Pacific herbivorous fish fauna is the result of ongoing lineage expansion that started in the central Tethys. The Atlantic is a composite fauna with just one endemic lineage and at least four colonization events from the Indo‐Pacific.
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