Luke Tornabene

Evolution of microhabitat association and morphology in a diverse group of cryptobenthic coral reef fishes (Teleostei: Gobiidae: Eviota)

Gobies (Teleostei: Gobiidae) are an extremely diverse and widely distributed group and are the second most species rich family of vertebrates. Ecological drivers are key to the evolutionary success of the Gobiidae. However, ecological and phylogenetic data are lacking for many diverse genera of gobies. Our study investigated the evolution of microhabitat association across the phylogeny of 18 species of dwarfgobies (genus Eviota), an abundant and diverse group of coral reef fishes. In addition, we also explore the evolution of pectoral fin-ray branching and sensory head pores to determine the relationship between morphological evolution and microhabitat shifts. Our results demonstrate that Eviota species switched multiple times from a facultative hard-coral association to inhabiting rubble or mixed sand/rubble habitat. We found no obvious relationship between microhabitat shifts and changes in pectoral fin-ray branching or reduction in sensory pores, with the latter character being highly homoplasious throughout the genus. The relative flexibility in coral-association in Eviota combined with the ability to move into non-coral habitats suggests a genetic capacity for ecological release in contrast to the strict obligate coral-dwelling relationship commonly observed in closely related coral gobies, thus promoting co-existence through fine scale niche partitioning. The variation in microhabitat association may facilitate opportunistic ecological speciation, and species persistence in the face of environmental change. This increased speciation opportunity, in concert with a high resilience to extinction, may explain the exceptionally high diversity seen in Eviota compared to related genera in the family.

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.

Varicus lacerta, a new species of goby (Teleostei, Gobiidae, Gobiosomatini, Nes subgroup) from a mesophotic reef in the southern Caribbean

Abstract We describe a new species of goby, Varicus lacerta sp. n., which was collected from a mesophotic reef at Curacao, southern Caribbean. The new species is the tenth species of Varicus, all of which occur below traditional SCUBA depths in the wider Caribbean area. Its placement in the genus Varicus is supported by a molecular phylogenetic analysis of three nuclear genes and the mitochondrial gene cytochrome b. In addition, the new species has one anal-fin pterygiophore inserted anterior to the first haemal spine, which distinguishes Varicus species from most species in the closely related and morphologically similar genus Psilotris. Varicus lacerta sp. n. is distinguished from all other named species of Varicus by the absence of scales, having highly branched, feather-like pelvic-fin rays, and in its live coloration. We provide the cytochrome c oxidase I DNA barcode of the holotype and compare color patterns of all species of Varicus and Psilotris for which color photographs or illustrations are available. This study is one of several recent studies demonstrating the utility of manned submersibles in exploring the diversity of poorly studied but species-rich deep-reef habitats.

Two new deep-reef basslets (Teleostei, Grammatidae, Lipogramma), with comments on the eco-evolutionary relationships of the genus

Abstract The banded basslet, Lipogramma evides Robins & Colin, 1979, is shown to comprise two species: Lipogramma evides, which inhabits depths of 133–302 m, and a new species described here as Lipogramma levinsoni, which inhabits depths of 108–154 m and previously was considered to represent the juvenile of Lipogramma evides. A second new species of banded basslet, described here as Lipogramma haberi, inhabits depths of 152–233 m and was previously not reported in the literature. Morphologically, the three species differ in color patterns and modal numbers of gill rakers, whereas various other morphological features distinguish Lipogramma levinsoni from Lipogramma evides and Lipogramma haberi. DNA barcode data and multilocus, coalescent-based, species-delimitation analysis support the recognition of the three species. Phylogenetic analysis of mitochondrial and nuclear genetic data supports a sister-group relationship between the two deepest-living of the three species, Lipogramma evides and Lipogramma haberi, and suggests that the shallower Lipogramma levinsoni is more closely related to Lipogramma anabantoides Böhlke, 1960, which inhabits depths < 120 m. Evolutionary relationships within Lipogramma thus appear to be correlated with species depth ranges, an eco-evolutionary pattern that has been observed in other Caribbean marine teleosts and that warrants further investigation. The new species represent the eleventh and twelfth new fish species described in recent years from exploratory submersible diving in the Caribbean in the globally poorly studied depth zone of 50–300 m. This study suggests that there are at least two additional cryptic species of Lipogramma, which are being analyzed in ongoing investigations of Caribbean deep-reef ecosystems.

Four new species of dwarfgobies (Teleostei: Gobiidae: Eviota) from the Austral, Gambier, Marquesas and Society Archipelagos, French Polynesia

Four new species of Eviota (Teleostei: Gobiidae) are described from French Polynesia. Eviota hinanoae occurs from the Gambier, Austral and Society Archipelagos and differs from its closest relatives primarily in sensory pore pattern, having cuplike male urogenital papilla, and in lacking prominent dark pigmentation on the base of the pectoral fin. Three other new species, E. dorsimaculata, E. lacrimosa and E. deminuta, are known only from the Marquesas Islands and are distinguished from congeners by differences in pigmentation, sensory pore pattern, urogenital papilla shape, the number of rays in the dorsal and anal fins, and the length of the fifth pelvic-fin ray. Eviota deminuta represents one of the smallest known species of Eviota and features reductions in several morphological characters, including the loss of all head pores. Three of the new species are included in a phylogenetic analysis based on mitochondrial cytochrome c oxidase-I, along with 21 additional species of Eviota.

Eviota brahmi n. sp. from Papua New Guinea, with a redescription of Eviota nigriventris (Teleostei: Gobiidae).

Greenfield & Randall (2011) described the gobiid fishes Eviota dorsogilva from Fiji and E. dorsopurpurea from Papua New Guinea as new species in what they termed the Eviota nigriventris complex. They also extended the range of E. nigriventris, type locality Banda Sea, to Milne Bay, Papua New Guinea. In the present paper, we describe their misidentified E. nigriventris from Papua New Guinea as a new species, E. brahmi, and redescribe E. nigriventris based on new material from near the type locality. The four species of this complex differ mainly in coloration, but are also shown to be distinct using mitochondrial and nuclear DNA.

A new mesophotic goby, Palatogobius incendius (Teleostei: Gobiidae), and the first record of invasive lionfish preying on undescribed biodiversity

A new species of deep-reef fish in the goby genus Palatogobius is described from recent submersible collections off Curaçao and Dominica. Video footage of schools of this species reveal predation by the invasive Indo-Pacific lionfish (Pterois spp.), the first record of undescribed fauna potentially being eaten by lionfish outside of its native range. We present molecular phylogenetic data for all valid species of Palatogobius and related genera, as well as a taxonomic key to the species of Palatogobius and a generic key to Palatogobius and related genera in the western Atlantic. Lastly, we discuss ecological and behavioral aspects of some deep-reef fishes in light of potential threats from invasive lionfish.

Status of Gobiosoma (Teleostei: Gobiidae) from Brazil: description of a new species, redescription of G. hemigymnum , molecular phylogeny of the genus, and key to Atlantic species

It is unclear how many species of Gobiosoma occur in Brazil and what their geographic distributions are. Here we combine data from a comprehensive morphological survey and a molecular analysis to clarify this uncertain taxonomy and place Brazilian Gobiosoma within a phylogenetic framework. Recent collections in Brazil, from the states of Ceará to Santa Catarina, and in Uruguay yielded two allopatric species of Gobiosoma that are distinct in genetics, meristics, morphometrics, scale pattern and coloration. Comparisons were made with types and specimens of Gobiosoma hemigymnum, Garmannia mediocricula, Gobiosoma spilotum and Gobiosoma parri and all other known species of Gobiosoma. We place G. parri in synonomy with G. hemigymnum with a distribution of Rio de Janeiro to Uruguay and Argentina. The northern species, that extends from the states of Espírito Santo to Ceará, is described as a new species, Gobiosoma alfiei. A key to the Atlantic species of Gobiosoma is provided.

Below the Mesophotic

Mesophotic coral ecosystems, which occur at depths of ~40 to 150 m, have received recent scientific attention as potential refugia for organisms inhabiting deteriorating shallow reefs. These ecosystems merit research in their own right, as they harbor both depth-generalist species and a distinctive reef-fish fauna. Reef ecosystems just below the mesophotic are globally underexplored, and the scant recent literature that mentions them often suggests that mesophotic ecosystems transition directly into those of the deep sea. Through submersible-based surveys in the Caribbean Sea, we amassed the most extensive database to date on reef-fish diversity between ~40 and 309 m at any single tropical location. Our data reveal a unique reef-fish assemblage living between ~130 and 309 m that, while taxonomically distinct from shallower faunas, shares strong evolutionary affinities with them. Lacking an existing name for this reef-faunal zone immediately below the mesophotic but above the deep aphotic, we propose “rariphotic.” Together with the “altiphotic,” proposed here for the shallowest reef-faunal zone, and the mesophotic, the rariphotic is part of a depth continuum of discrete faunal zones of tropical reef fishes, and perhaps of reef ecosystems in general, all of which warrant further study in light of global declines of shallow reefs.

The relative importance of regional, local, and evolutionary factors structuring cryptobenthic coral-reef assemblages

Factors shaping coral-reef fish species assemblages can operate over a wide range of spatial scales (local versus regional) and across both proximate and evolutionary time. Niche theory and neutral theory provide frameworks for testing assumptions and generating insights about the importance of local versus regional processes. Niche theory postulates that species assemblages are an outcome of evolutionary processes at regional scales followed by local-scale interactions, whereas neutral theory presumes that species assemblages are formed by largely random processes drawing from regional species pools. Indo-Pacific cryptobenthic coral-reef fishes are highly evolved, ecologically diverse, temporally responsive, and situated on a natural longitudinal diversity gradient, making them an ideal group for testing predictions from niche and neutral theories and effects of regional and local processes on species assemblages. Using a combination of ecological metrics (fish density, diversity, assemblage composition) and evolutionary analyses (testing for phylogenetic niche conservatism), we demonstrate that the structure of cryptobenthic fish assemblages can be explained by a mixture of regional factors, such as the size of regional species pools and broad-scale barriers to gene flow/drivers of speciation, coupled with local-scale factors, such as the relative abundance of specific microhabitat types. Furthermore, species of cryptobenthic fishes have distinct microhabitat associations that drive significant differences in assemblage community structure between microhabitat types, and these distinct microhabitat associations are phylogenetically conserved over evolutionary timescales. The implied differential fitness of cryptobenthic fishes across varied microhabitats and the conserved nature of their ecology are consistent with predictions from niche theory. Neutral theory predictions may still hold true for early life-history stages, where stochastic factors may be more important in explaining recruitment. Overall, through integration of ecological and evolutionary techniques, and using multiple spatial scales, our study offers a unique perspective on factors determining coral-reef fish assemblages.