A multi-locus approach to elucidating the evolutionary history of the clingfish Tomicodon petersii (Gobiesocidae) in the Tropical Eastern Pacific.

Marine species that are widely distributed in the Tropical Eastern Pacific (TEP) has served as a model for studying biogeographic patterns resulting from the effects of intraregional habitat discontinuities and oceanographic processes on the diversification and evolution of cryptobenthic reef fishes. Tomicodon petersii, a clingfish (Gobiesocidae) endemic to the TEP, is found on very shallow rocky reefs from central Mexico to northern Peru, and in the Cocos and Galapagos islands. We evaluated the effect of likely biogeographic barriers in different parts of the TEP on the diversification process of this species. We used one mitochondrial and three nuclear DNA markers from 112 individuals collected across the distribution range of T. petersii. Our phylogenetic results showed the samples constituted a monophyletic group, with three well-supported, allopatric subgroups: in the Mexican province, the Panamic province (from El Salvador to Ecuador), and the Galapagos Islands. The split between the Mexican and more southerly clades was estimated to occur at the end of the Miocene ca. 5.74 Mya, and the subsequent cladogenetic event separating the Galapagos population from the Panamic population at the junction of the Pliocene and Pleistocene, ca. 2.85 Mya. The species tree, Bayesian species delimitation tests (BPP), STACEY, and substantial genetic distances separating these three populations indicate that these three independent evolutionary units likely include two unnamed species. The cladogenetic events that promoted the formation of those genetically differentiated groups are consistent with disruptive effects on gene flow of habitat discontinuities and oceanographic processes along the mainland shoreline in the TEP and of ocean-island isolation, in conjunction with the species intrinsic life-history characteristics.

Evolutionary origin of the Atlantic Cabo Verde nibbler (Girella stuebeli), a member of a primarily Pacific Ocean family of antitropical herbivorous reef fishes.

Nibblers (family Girellidae) are reef fishes that are mostly distributed in the Indo-Pacific, with one exception: Girella stuebeli, which is found in the Cabo Verde Archipelago, in the Atlantic Ocean. We capitalized on this unusual distribution to study the evolutionary history of the girellids, and determine the relationship between G. stuebeli and the remaining nibbler taxa. Based on thousands of genomic markers (RAD sequences), we identified the closest relatives of G. stuebeli as being a clade of three species endemic to the northwestern Pacific, restricted to the Sea of Japan and vicinity. This clade diverged from G. stuebeli approximately 2.2 Mya. Two alternative potential routes of migration may explain this affinity: a western route, from the Tropical Eastern Pacific and the Tropical Western Atlantic, and an eastern route via the Indian Ocean and Southern Africa. The geological history and oceanography of the regions combined with molecular data presented here, suggest that the eastern route of invasion (via the Indian Ocean and Southern Africa) is a more likely scenario.

Phylogenetics and geography of speciation in New World Halichoeres wrasses.

The New World Halichoeres comprises about 30 small to medium sized wrasse species that are prominent members of reef communities throughout the tropical Western Atlantic and Eastern Pacific. We conducted a phylogenetic analysis of this group and related lineages using new and previously published sequence data. We estimated divergence times, evaluated the monophyly of this group, their relationship to other labrids, as well as the time-course and geography of speciation. These analyses show that all members of New World Halichoeres form a monophyletic group that includes Oxyjulis and Sagittalarva. New World Halichoeres is one of numerous labrid groups that appear to have radiated rapidly about 32 Ma and form a large polytomy within the julidine wrasses. We reconstruct the tropical Western Atlantic to be the ancestral area of New World Halichoeres, with four invasions of the Eastern Pacific and one reversal from East Pacific to Western Atlantic. These five speciation events were spread across the history of the group, with none corresponding closely to the time of the closure of the Isthmus of Panama. Three speciation events within the Atlantic occurred across the Orinoco-Amazon outflow and within the Pacific, five involve splits between lineages that occupy coastal reef systems and offshore islands. Of eight sister species pairs, seven show complete allopatry and one is fully sympatric.

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.

Adult and larval traits as determinants of geographic range size among tropical reef fishes.

Most marine organisms disperse via ocean currents as larvae, so it is often assumed that larval-stage duration is the primary determinant of geographic range size. However, empirical tests of this relationship have yielded mixed results, and alternative hypotheses have rarely been considered. Here we assess the relative influence of adult and larval-traits on geographic range size using a global dataset encompassing 590 species of tropical reef fishes in 47 families, the largest compilation of such data to date for any marine group. We analyze this database using linear mixed-effect models to control for phylogeny and geographical limits on range size. Our analysis indicates that three adult traits likely to affect the capacity of new colonizers to survive and establish reproductive populations (body size, schooling behavior, and nocturnal activity) are equal or better predictors of geographic range size than pelagic larval duration. We conclude that adult life-history traits that affect the postdispersal persistence of new populations are primary determinants of successful range extension and, consequently, of geographic range size among tropical reef fishes.

Two new species of Varicus from Caribbean deep reefs, with comments on the related genus Pinnichthys (Teleostei, Gobiidae, Gobiosomatini, Nes subgroup).

Tropical deep reefs (~40-300 m) are diverse ecosystems that serve as habitats for diverse communities of reef-associated fishes. Deep-reef fish communities are taxonomically and ecologically distinct from those on shallow reefs, but like those on shallow reefs, they are home to a species-rich assemblage of small, cryptobenthic reef fishes, including many species from the family Gobiidae (gobies). Here we describe two new species of deep-reef gobies, Varicusprometheussp. nov. and V.roatanensissp. nov., that were collected using the submersible Idabel from rariphotic reefs off the island of Roatan (Honduras) in the Caribbean. The new species are the 11th and 12th species of the genus Varicus, and their placement in the genus is supported by morphological data and molecular phylogenetic analyses. Additionally, we also collected new specimens of the closely-related genus and species Pinnichthysaimoriensis during submersible collections off the islands of Bonaire and St. Eustatius (Netherland Antilles) and included them in this study to expand the current description of that species and document its range extension from Brazil into the Caribbean. Collectively, the two new species of Varicus and new records of P.aimoriensis add to our growing knowledge of cryptobenthic fish diversity on deep reefs of the Caribbean.

Environmental DNA (eDNA) reveals potential for interoceanic fish invasions across the Panama Canal.

Interoceanic canals can facilitate biological invasions as they connect the world's oceans and remove dispersal barriers between bioregions. As a consequence, multiple opportunities for biotic exchange arise and the resulting establishment of migrant species often causes adverse ecological and economic impacts. The Panama Canal is a key region for biotic exchange as it connects the Pacific and Atlantic Oceans in Central America. In this study, we used two complementary methods (environmental DNA (eDNA) metabarcoding and gillnetting) to survey fish communities in this unique waterway. Using COI (cytochrome oxidase subunit I) metabarcoding, we detected a total of 142 fish species, including evidence for the presence of sixteen Atlantic and eight Pacific marine fish in different freshwater sections of the Canal. Of these, nine are potentially new records. Molecular data did not capture all species caught with gillnets, but generally provided a more complete image of the known fish fauna as more small-bodied fish species were detected. Diversity indices based on eDNA surveys revealed significant differences across different sections of the Canal reflecting in part the prevailing environmental conditions. The observed increase in the presence of marine fish species in the Canal indicates a growing potential for interoceanic fish invasions. The potential ecological and evolutionary consequences of this increase in marine fishes are not only restricted to the fish fauna in the Canal as they could also impact adjacent ecosystems in the Pacific and Atlantic Oceans.

Generic reassignment of Centropristis fuscula Poey, 1861 (Teleostei: Serranidae), with re-description of the species and comments on its geographical range and sexual system.

Centropristes fusculus Poey, 1861 historically has variously and somewhat perplexingly been assigned to Centropristis Cuvier, 1829, Prionodes Jenyns, 1840, and Serranus Cuvier, 1816. Here, we provide evidence from comparisons of morphology, ecology, and sexual systems for its inclusion in Serranus and redescribe the species based on the holotype and 60 specimens from Brazil, the Caribbean, the United States, and Uruguay. Serranus fusculus is a simultaneous hermaphrodite, a sexual system that is relevant to its generic placement. The inclusion of Serranus fusculus in the genus Serranus increases to 33 the number of currently valid Serranus species, of which two are found in the Western Indian Ocean, six in the eastern Pacific and 25 in the Atlantic Ocean (15 restricted to the western Atlantic and 10 to the eastern and Central Atlantic). An identification key to western Atlantic species of the genus is provided.

Ecological traits influencing range expansion across large oceanic dispersal barriers: insights from tropical Atlantic reef fishes.

How do biogeographically different provinces arise in response to oceanic barriers to dispersal? Here, we analyse how traits related to the pelagic dispersal and adult biology of 985 tropical reef fish species correlate with their establishing populations on both sides of two Atlantic marine barriers: the Mid-Atlantic Barrier (MAB) and the Amazon-Orinoco Plume (AOP). Generalized linear mixed-effects models indicate that predictors for successful barrier crossing are the ability to raft with flotsam for the deep-water MAB, non-reef habitat usage for the freshwater and sediment-rich AOP, and large adult-size and large latitudinal-range for both barriers. Variation in larval-development mode, often thought to be broadly related to larval-dispersal potential, is not a significant predictor in either case. Many more species of greater taxonomic diversity cross the AOP than the MAB. Rafters readily cross both barriers but represent a much smaller proportion of AOP crossers than MAB crossers. Successful establishment after crossing both barriers may be facilitated by broad environmental tolerance associated with large body size and wide latitudinal-range. These results highlight the need to look beyond larval-dispersal potential and assess adult-biology traits when assessing determinants of successful movements across marine barriers.

A review of 263 years of taxonomic research on Hypoplectrus (Perciformes: Serranidae), with a redescription of Hypoplectrus affinis (Poey, 1861).

The hamlets (Hypoplectrus spp., Perciformes: Serranidae) constitute a distinctive model system for the study of a variety of ecological and evolutionary processes including the evolution and maintenance of simultaneous hermaphroditism and egg trading, sex allocation, sexual selection, social-trap, mimicry, dispersal, speciation, and adaptive radiation. Addressing such fundamental and complex processes requires a good knowledge of the taxonomy and natural history of the hamlets. Here, we review the taxonomy of the hamlets, from early ichthyological studies to the most recent species description in 2018. We report a total of 72 different binomial names for Hypoplectrus, synonymized or invalidated down to 17 unambiguously recognized species today. In addition, we redescribe Hypoplectrus affinis (Poey, 1861) as a valid species. In Bocas del Toro (Panama), this hamlet is distinct from eight sympatric congeners in terms of colour pattern, body size and behaviour. Whole-genome analysis and spawning observations indicate that it is genetically distinct from sympatric congeners and reproductively isolated through assortative pairing. Based on the colour pattern we detail in its redescription, live-fish photographs, videos, and earlier reports, H. affinis occurs in Panama, Nicaragua, Mexico, the Florida Keys, Cuba, Grand Cayman, Jamaica, the Dominican Republic, Los Roques (Venezuela), Bonaire, and Tobago. We conclude with a discussion of pending taxonomic issues in this group and the species status of the hamlets in general.

An updated, illustrated inventory of the marine fishes of the US Virgin Islands.

The US Virgin Islands (USVI) include St. John and St. Thomas on the Puerto Rican Platform (PRP) and St. Croix, isolated by 2000 m deep water 45 km south of that platform. Previous inventories of the marine fishes of these islands include a comprehensive 2014 checklist of the fishes of St. Croix and a list of the fishes of the PRP produced in 2000. The latter list noted the locations of many records of the plateau's fishes, allowing the construction of a combined inventory for St. John and St. Thomas. Those two islands are treated here as a single faunal unit because they are only 3.5 km apart on a shared shallow shelf with various islets and reefs in between. Here we provide updated information on those two USVI (St. Croix and St. John-Thomas) marine fish faunas. The additions to the St. Croix and St. John-Thomas inventories presented here are based on a combination of information from the two sources indicated above, more recent publications dealing with those faunas, a review of location records on various online sources of biogeographic data, and voucher photographs taken of fishes in the field by authors of this paper and other citizen scientists. This assessment increased the known fauna of St. Croix by 7.5% to 585 species. The inventory for St. John-Thomas increased by 39.9% from 401 species on the 2000 PRP list to 561 with the inclusion of records from other sources. On-site mtDNA (COI) barcodes are available for approximately one-third of the species of the St. John-Thomas fauna, but for only one species collected at St. Croix. A set of underwater photographs of 372 species (34 of them representing the sole record of a species) from St. John-Thomas and of 11 shallow-water species added to the St. Croix fauna is included. These represent occurrence vouchers and also are intended to facilitate future work that builds on the present compendium.

The origin of the parrotfish species Scarus compressus in the Tropical Eastern Pacific: region-wide hybridization between ancient species pairs.

BACKGROUND: In the Tropical Eastern Pacific (TEP), four species of parrotfishes with complex phylogeographic histories co-occur in sympatry on rocky reefs from Baja California to Ecuador: Scarus compressus, S. ghobban, S. perrico, and S. rubroviolaceus. The most divergent, S. perrico, separated from a Central Indo-Pacific ancestor in the late Miocene (6.6 Ma). We tested the hypothesis that S. compressus was the result of ongoing hybridization among the other three species by sequencing four nuclear markers and a mitochondrial locus in samples spanning 2/3 of the latitudinal extent of the TEP. RESULTS: A Structure model indicated that K = 3 fit the nuclear data and that S. compressus individuals had admixed genomes. Our data could correctly detect and assign pure adults and F1 hybrids with > 0.90 probability, and correct assignment of F2s was also high in some cases. NewHybrids models revealed that 89.8% (n = 59) of the S. compressus samples were F1 hybrids between either S. perrico × S. ghobban or S. perrico × S. rubroviolaceus. Similarly, the most recently diverged S. ghobban and S. rubroviolaceus were hybridizing in small numbers, with half of the admixed individuals assigned to F1 hybrids and the remainder likely > F1 hybrids. We observed strong mito-nuclear discordance in all hybrid pairs. Migrate models favored gene flow between S. perrico and S. ghobban, but not other species pairs. CONCLUSIONS: Mating between divergent species is giving rise to a region-wide, multispecies hybrid complex, characterized by a high frequency of parental and F1 genotypes but a low frequency of > F1 hybrids. Trimodal structure, and evidence for fertility of both male and female F1 hybrids, suggest that fitness declines sharply in later generation hybrids. In contrast, the hybrid population of the two more recently diverged species had similar frequencies of F1 and > F1 hybrids, suggesting accelerating post-mating incompatibility with time. Mitochondrial genotypes in hybrids suggest that indiscriminate mating by male S. perrico is driving pre-zygotic breakdown, which may reflect isolation of this endemic species for millions of years resulting in weak selection for conspecific mate recognition. Despite overlapping habitat use and high rates of hybridization, species boundaries are maintained by a combination of pre- and post-mating processes in this complex.

Molecular phylogenetics and evolution of Holacanthus angelfishes (Pomacanthidae).

The angelfish genus Holacanthus includes seven species in the tropical Eastern Pacific and Atlantic. In this study we performed an analysis on all species, the closely related regal angelfish, and the Cortez angelfish, using four mitochondrial and one nuclear marker. Our results support a monophyletic Holacanthus. The Indo-Pacific regal angelfish, Pygoplytes diacanthus, was found to be the closest relative to Holacanthus. We found a split into two clades with divergences that were consistent with the rise of the Isthmus of Panama. An internally calibrated molecular clock thus placed the origin of Holacanthus to approximately 10.2-7.6 million years ago.

Misidentification of Bellator gymnostethus (Gilbert, 1892) as Prionotus ruscarius Gilbert amp; Starks, 1904 (Scorpaeniformes: Triglidae).

The checklist by Robertson et al. (2017) of fishes from the tropical eastern Pacific included information on three members of the family Triglidae: Bellator loxias (Jordan, 1897), Prionotus ruscarius and P. stephanophrys Lockington, 1881. Unfortunately, the identification of four specimens as P. ruscarius is incorrect, as they are Bellator gymnostethus. We thank Benjamin Victor for bringing these misidentifications to our notice through his work with mtDNA sequence data from the Barcode of Life Database (BOLD: http://www.boldsystems.org). The photographs of the four specimens on the BOLD website clearly depict a Bellator species rather than a Prionotus. However, the photograph in the 2017 paper (Figure 75, page 78), is correctly identified and labelled as P. ruscarius, and this species was collected on the cruise of the Miguel Oliver discussed in Robertson et al. (2017), see Benavides Moreno et al. (2019). This correction brings the number of triglids collected on that cruise to four species.

An update to the inventory of shore-fishes from the Parque Nacional Sistema Arrecifal Veracruzano, Veracruz, México.

Data on marine and brackish-water fishes recorded in the area of the Parque Nacional Sistema Arrecifal Veracruzano in the southwest Gulf of Mexico were extracted from online aggregators of georeferenced location records, the recent ichthyological literature reviewed, and collections and observations made to provide a more complete faunal inventory for that park. Those actions added 95 species to a comprehensive inventory published in 2013, and brought the total to 472 species, an increase of 22%. Seventy-four percent of the additions came from online aggregators of georeferenced species records, which clearly demonstrates the value of reviewing and incorporating such data into species inventories. However, different aggregators recorded different sets of species, and some of their data were linked to outdated taxonomy or included identification errors. Hence individual records from multiple aggregators need to be obtained and reviewed for such issues when using such data to compile and revise faunal inventories. Existing lists also need to be carefully reviewed to ensure that errors are not perpetuated during updates.

Reef-associated fishes from the offshore reefs of western Campeche Bank, Mexico, with a discussion of mangroves and seagrass beds as nursery habitats.

A series of small emergent coral reefs and shallow, submerged coralliferous banks are scattered along the western edge of Campeche Bank (southwest Gulf of Mexico), 150-200 km offshore from the Yucatán Peninsula, Mexico. Here a reasonably comprehensive, annotated checklist of reef-associated fishes for one reef, Cayo Arcas (expanded from 162 to 209 species) is presented, with preliminary checklists of such fishes from three other emergent reefs (Cayo Arenas, Triángulo Oeste, Triángulo Este) and four submerged bank reefs (Banco Obispo Norte, Banco Obispo Sur, Banco Nuevo and Banco Pera). During 2017-18 a total of 260 species was observed or collected from those reefs, and previous studies and georeferenced museum records in the global aggregator Fishnet2 added another 101 shallow-living species recorded on or adjacent to those reefs. Some coral-reef fishes are thought to be strongly dependent on seagrass and mangrove areas as nursery habitats for maintenance of their local populations on reefs near to those habitats. The abundance of a number of such "nursery" species on these Campeche reefs indicates otherwise, as there are no seagrass- or mangrove habitats for reef fishes within ~ 150 km of the study reefs. Other isolated Caribbean-area reefs that lack mangroves and, in some cases, seagrasses, also support many such nursery species of reef-fishes.

Comparative phylogeography of Atlantic reef fishes indicates both origin and accumulation of diversity in the Caribbean.

BACKGROUND: Two processes may contribute to the formation of global centers of biodiversity: elevated local speciation rates (the center of origin hypothesis), and greater accumulation of species formed elsewhere (the center of accumulation hypothesis). The relative importance of these processes has long intrigued marine biogeographers but rarely has been tested. RESULTS: To examine how origin and accumulation affected the Greater Caribbean center of diversity, we conducted a range-wide survey of mtDNA cytochrome b in the widespread Atlantic reef damselfish Chromis multilineata (N = 183) that included 10 locations in all four tropical Atlantic biogeographic provinces: the Greater Caribbean, Brazil, the mid-Atlantic ridge, and the tropical eastern Atlantic. We analyzed this data and re-evaluated published genetic data from other reef fish taxa (wrasses and parrotfishes) to resolve the origin and dispersal of mtDNA lineages. Parsimony networks, mismatch distributions and phylogenetic analyses identify the Caribbean population of C. multilineata as the oldest, consistent with the center of origin model for the circum-Atlantic radiation of this species. However, some Caribbean haplotypes in this species were derived from Brazilian lineages, indicating that mtDNA diversity has not only originated but also accumulated in the Greater Caribbean. Data from the wrasses and parrotfishes indicate an origin in the Greater Caribbean in one case, Caribbean origin plus accumulation in another, and accumulation in the remaining two. CONCLUSION: Our analyses indicate that the Greater Caribbean marine biodiversity hotspot did not arise through the action of a single mode of evolutionary change. Reef fish distributions at the boundaries between Caribbean and Brazilian provinces (the SE Caribbean and NE Brazil, respectively) indicate that the microevolutionary patterns we detected in C. multilineata and other reef fishes translate into macroevolutionary processes and that origin and accumulation have acted in concert to form the Greater Caribbean biodiversity hotspot.

A new species of Lipogramma from deep reefs of Roatan, Honduras (Teleostei, Grammatidae).

A new species of Lipogramma is described from submersible collections at 122-165 m depth off the coast of Roatan, Honduras, in the western Caribbean. The new species is distinguished from all other species in the genus by its bright blue coloration on the head, nape, and dorsal portion of the trunk beneath the spinous dorsal fin, a prominent round black blotch below the origin of the spinous dorsal fin, and a high number of gill rakers. A molecular phylogeny based on mitochondrial and nuclear genes shows that the new species belongs to a clade containing L.levinsoni, L.regia, and L.anabantoides. At Roatan, submersible observations of this and other Lipogramma species indicate clear, interspecific habitat partitioning by depth and substrate.

An Indo-Pacific damselfish (Neopomacentrus cyanomos) in the Gulf of Mexico: origin and mode of introduction.

The Indo-West Pacific (IWP) coral-reef damselfish Neopomacentrus cyanomos is well established across the south-west Gulf of Mexico (SwGoMx). Comparisons of mtDNA sequences of the SwGoMx population with those from conspecifics from 16 sites scattered across its native geographic range show that the SwGoMx population is derived from two of four native lineages: one from the north-west Pacific Ocean, the other from the northern Indian Ocean. Three hypotheses address how this species was introduced to the SwGoMX: (1) aquarium release; (2) borne by cargo-ship; and (3) carried by offshore petroleum platform (petro-platform). The first is unlikely because this species rarely features in the aquarium trade, and "N. cyanomos" traded to the USA from the sole IWP source we are aware of are a misidentified congener, N. taeniurus. The second hypothesis is unlikely because shipping has not been associated with the introduction of alien damselfishes, there is little international shipping between the IWP and the SwGoMx, and voyages between those areas would be lengthy and along environmentally unfavorable routes. Various lines of evidence support the third hypothesis: (i) bio-fouled petro-platforms represent artificial reefs that can sustain large and diverse populations of tropical reef-fishes, including N. cyanomos in the SwGoMx; (ii) relocation of such platforms has been implicated in trans-oceanic introductions leading to establishment of non-native populations of such fishes; and (iii) genetic characteristics of the SwGoMx population indicate that it was established by a large and diverse group of founders drawn from the IWP regions where many petro-platforms currently in the SwGoMx and other Atlantic offshore oilfields originated.