Christine E. Thacker

Molecular phylogeny of the gobioid fishes (Teleostei: Perciformes: Gobioidei).

The phylogeny of groups within Gobioidei is examined with molecular sequence data. Gobioidei is a speciose, morphologically diverse group of teleost fishes, most of which are small, benthic, and marine. Efforts to hypothesize relationships among the gobioid groups have been hampered by the prevalence of reductive evolution among goby species; such reduction can make identification of informative morphological characters particularly difficult. Gobies have been variously grouped into two to nine families, several with included subfamilies, but most existing taxonomies are not phylogenetic and few cladistic hypotheses of relationships among goby groups have been advanced. In this study, representatives of eight of the nine gobioid familes (Eleotridae, Odontobutidae, Xenisthmidae, Gobiidae, Kraemeriidae, Schindleriidae, Microdesmidae, and Ptereleotridae), selected to sample broadly from the range of goby diversity, were examined. Complete sequence from the mitochondrial ND1, ND2, and COI genes (3573 bp) was used in a cladistic parsimony analysis to hypothesize relationships among the gobioid groups. A single most parsimonious topology was obtained, with decay indices indicating strong support for most nodes. Major phylogenetic conclusions include that Xenisthmidae is part of Eleotridae, and Eleotridae is paraphyletic with respect to a clade composed of Gobiidae, Microdesmidae, Ptereleotridae, Kraemeriidae, and Schindleriidae. Within this five-family clade, two clades are recovered. One includes Gobionellinae, which is paraphyletic with respect to Kraemeriidae, Sicydiinae, Oxudercinae, and Amblyopinae. The other contains Gobiinae, also paraphyletic, and including Microdesmidae, Ptereleotridae, and Schindleriidae. Previous morphological evidence for goby groupings is discussed; the phylogenetic hypothesis indicates that the morphological reduction observed in many goby species has been derived several times independently.

Phylogeny of Gobioidei and Placement within Acanthomorpha, with a New Classification and Investigation of Diversification and Character Evolution

Abstract Phylogenies based on DNA sequence data are providing a range of new insights into relationships within Acanthomorpha, particularly in cases where morphological characters have been scanty or misleading. Molecular phylogenetic analyses of the perciform suborder Gobioidei have illuminated relationships within and among groups, with recovered clades generally corresponding to groups identified based on morphological characters. This study integrates and expands previous molecular phylogenetic hypotheses to infer a comprehensive gobioid phylogeny, including a variety of outgroup taxa included to confirm sister taxon identity and position of the group among other acanthomorphs. This and other phylogenetic hypotheses indicate that Gobioidei is part of a clade that also includes Apogonidae, Pempheridae, and Kurtidae. These groups share characteristics of the skeleton, soft tissues, and reproductive ecology. A new six-family clade-based classification of Gobioidei is presented, and Gobioidei, Apogonoidei (Apogonidae + Pempheridae), and Kurtoidei are placed as suborders of a resurrected Gobiiformes. Patterns of morphological character evolution among gobioids are then examined in the context of the molecular phylogeny, and their distribution is correlated with species diversification and phylogenetic imbalance. The two largest gobioid clades, Gobiidae and Gobionellidae, differ significantly in species richness, perhaps due to increased diversification in marine habitats by gobiids. The phylogeny of Gobiidae exhibits a convex plot of lineages through time, consistent with an elevation of speciation rate early in the clades history. The γ statistic is consistent with this increase, but is not significant after correction with the Monte Carlo Constant Rates (MCCR) test.

Phylogeny of Gobiidae and identification of gobiid lineages

The teleost family Gobiidae includes at least 1120 described species of fishes, distributed worldwide in both tropical and temperate habitats. The majority of gobies inhabit marine environments, in particular Old World coral reefs. However, a radiation of gobiids inhabits the rivers and near-shore habitats of Europe and Asia, and a variety of genera are also found in the seas of the New World. This study builds on previous work in which gobiids were placed among their gobioid relatives by adding additional taxa as well as additional markers, providing a much more comprehensive portrait of gobiid intrarelationships and including all major lineages of gobies. We used DNA sequences from both mitochondrial (ND1, ND2, COI) and nuclear (RAG2, Rhodopsin, RNF213) genes to infer phylogeny among 127 representatives of 100 species of gobies, using two gobionellid species as outgroups. We delineated 13 lineages within Gobiidae, including one clade of shrimp-associated gobies represented by the genera Cryptocentrus, Mahidolia and Stonogobiops and a second separate shrimp-associated goby clade including Amblyeleotris, Ctenogobiops and Vanderhorstia. The Mediterranean, Ponto-Caspian and Eastern Atlantic gobies are resolved in a clade along with two genera known from the Western Indian Ocean. Invasion of the New World is shown to have occurred multiple times among the sampled taxa, in the American seven-spined gobies, the Coryphopterus, Lophogobius and Rhinogobiops radiation (sister to Fusigobius) and separately in the wormfishes Cerdale and Microdesmus, resolved in a clade alongside the Indo-Pacific Gunnellichthys, Ptereleotris and Nemateleotris. The cosmopolitan genera Bathygobius and Priolepis represent further separate radiations, and Lythrypnus shows complex relationships with both Priolepis and Trimma.

Phylogeography of marine mutualists: parallel patterns of genetic structure between obligate goby and shrimp partners

The survival of many organisms depends on interspecific, mutualistic interactions. Hence, it is important to assess the phylogeography of multiple mutualistic species simultaneously to gain insight into how their metapopulations persist, spread and recover from disturbance. Consequently, we sequenced mitochondrial DNA (cytochrome b) from a gobiid fish (Ctenogobiops feroculus) and its mutualistic partner, an alpheid snapping shrimp (Alpheus djeddensis). These obligate mutualists are common in shallow coral reef lagoons, and we collected individuals from 11 Indo‐Pacific islands that were likely exposed to different disturbance histories due to sea level fluctuations associated with glaciation events [geological studies indicate that eastern oceanic islands (Cook Islands, French Polynesia) were more disturbed than western continental plate islands that have deeper, more extensive lagoons (Okinawa, Fiji)]. Both phylogenetic and population genetic analyses indicated that gobies from Okinawa and Fiji were genetically distinct both from each other and those in the Cook Islands and French Polynesia. Shrimp, by contrast, grouped into two distinct genetic groups that showed no geographic structure. Restricting the analysis to one clade of shrimp, which contained two‐thirds of the individuals, showed that these shrimp had very similar phylogeographical structure to the gobies. Mismatch distributions demonstrated that both gobies and shrimp experienced a recent, rapid population expansion into French Polynesia. Finally, nucleotide and haplotype diversities per sample location were significantly correlated between mutualists and tended to be higher on western continental than eastern oceanic islands. Our results suggest that these mutualists recovered from a major disturbance by colonizing South Pacific islands in synchrony.

Phylogeny of the Wormfishes (Teleostei: Gobioidei: Microdesmidae)

Abstract Microdesmidae (sensu stricto) includes 30 species of elongate, cryptic, benthic gobioid fishes. The phylogenetic relationships among microdesmid species have been unknown, and the sister taxon to Microdesmidae has been a matter of debate. In this study, the relationships of microdesmid species are hypothesized based on morphological characters, analyzed with cladistic parsimony methods. Characters previously used as evidence for a sister-taxon relationship between Microdesmidae, s.s., and five genera classified as a subfamily (Ptereleotrinae) in an expanded Microdesmidae are reexamined and found to be invalid. Microdesmidae s.s. is restored, including only Cerdale, Clarkichthys, Microdesmus, Gunnellichthys, and Paragunnellichthys. Monophyly of the microdesmid genera is confirmed, and characters diagnosing each genus, and other clades revealed in this analysis, are discussed. The five genera formerly placed in Ptereleotrinae are referred to Ptereleotridae (incertae sedis within Gobioidei), bringing the total number of gobioid families to nine. Microdesmidae is also placed incertae sedis in Gobioidei; some sister-taxon candidates could be excluded based on the characters surveyed in this analysis, but among other gobioids, no clear sister taxon to Microdesmidae could be identified.

Phylogeny of cardinalfishes (Teleostei: Gobiiformes: Apogonidae) and the evolution of visceral bioluminescence.

The cardinalfishes (Apogonidae) are a diverse clade of small, mostly reef-dwelling fishes, for which a variety of morphological data have not yielded a consistent phylogeny. We use DNA sequence to hypothesize phylogenetic relationships within Apogonidae and among apogonids and other acanthomorph families, to examine patterns of evolution including the distribution of a visceral bioluminescence system. In conformance with previous studies, Apogonidae is placed in a clade with Pempheridae, Kurtidae, Leiognathidae, and Gobioidei. The apogonid genus Pseudamia is recovered outside the remainder of the family, not as sister to the superficially similar genus Gymnapogon. Species sampled from the Caribbean and Western Atlantic (Phaeoptyx, Astrapogon, and some Apogon species) form a clade, as do the larger-bodied Glossamia and Cheilodipterus. Incidence of visceral bioluminescence is found scattered throughout the phylogeny, independently for each group in which it is present. Examination of the fine structure of the visceral bioluminescence system through histology shows that light organs exhibit a range of morphologies, with some composed of complex masses of tubules (Siphamia, Pempheris, Parapriacanthus) and others lacking tubules but containing chambers formed by folds of the visceral epithelium (Acropoma, Archamia, Jaydia, and Rhabdamia). Light organs in Siphamia, Acropoma, Pempheris and Parapriacanthus are distinct from but connected to the gut; those in Archamia, Jaydia, and Rhabdamia are simply portions of the intestinal tract, and are little differentiated from the surrounding tissues. The presence or absence of symbiotic luminescent bacteria does not correlate with light organ structure; the tubular light organs of Siphamia and chambered tubes of Acropoma house bacteria, those in Pempheridae and the other Apogonidae do not.

Species and shape diversification are inversely correlated among gobies and cardinalfishes (Teleostei: Gobiiformes)

Gobies and their relatives are significant components of nearshore marine, estuarine, and freshwater fish faunas in both tropical and temperate habitats worldwide. They are remarkable for their ability to adapt to and diversify in a wide range of environments. Among gobiiform clades, species diversities vary widely, ranging from two species in Kurtidae to more than 1,000 species in Gobiidae. There is also great variation in head and body shape and in environmental preferences (fresh, brackish, or marine habitats). In this study, I used a time-calibrated molecular phylogeny, coupled with morphometric and comparative analyses, to examine evolutionary rates of both speciation and morphological diversification among gobiiform lineages. Projection of the phylogeny onto a shape-derived morphospace shows that Gobioidei is morphometrically distinct from its sister taxon Apogonoidei, but that families within Gobioidei overlap in morphospace. Analysis of species diversification rates indicates that three rate shifts have occurred over the evolutionary history of Gobiiformes. Relative to the other lineages, Kurtidae has exhibited a slowdown in speciation, whereas both Apogonidae and Gobiidae + Gobionellidae have experienced an increase in diversification. Comparative analyses show that in Apogonidae and Gobiidae + Gobionellidae, increased speciation is correlated with diminished rates of morphological diversification, differently manifested in either clade and among the various sublineages. The elevation in speciation rates and diminishment in rates of morphological change in both Apogonidae and the clade Gobiidae + Gobionellidae are correlated with shifts to oceanic habitats from freshwater. This pattern is the complement to that seen across the global radiation of acanthomorph fishes in which a decrease in species diversification is associated with an increase in morphological disparity.

Ecology and Evolution Affect Network Structure in an Intimate Marine Mutualism

Elucidating patterns and causes of interaction among mutualistic species is a major focus of ecology, and recent meta-analyses of terrestrial networks show that network-level reciprocal specialization tends to be higher in intimate mutualisms than in nonintimate mutualisms. It is largely unknown, however, whether this pattern holds for and what factors affect specialization in marine mutualisms. Here we present the first analysis of network specialization () for marine mutualistic networks. Specialization among eight Indo-Pacific networks of obligate mutualistic gobies and shrimps was indistinguishable from that among comparably intimate terrestrial mutualisms (ants-myrmecophytes) and higher than that among nonintimate ones (seed dispersers). Specialization was affected by variability in habitat use for both gobies and shrimps and by phylogenetic history for shrimps. Habitat use was phylogenetically conserved among shrimp, and thus effects of shrimp phylogeny on partner choice were mediated in part by habitat. By contrast, habitat use and pairing patterns in gobies were not related to phylogenetic history. This asymmetry appears to result from evolutionary constraints on partner use in shrimps and convergence among distantly related gobies to utilize burrows provided by multiple shrimp species. Results indicate that the evolution of mutualism is affected by life-history characteristics that transcend environments and that different factors constrain interactions in disparate ecosystems.

Identification of the notothenioid sister lineage illuminates the biogeographic history of an Antarctic adaptive radiation

BackgroundAntarctic notothenioids are an impressive adaptive radiation. While they share recent common ancestry with several species-depauperate lineages that exhibit a relictual distribution in areas peripheral to the Southern Ocean, an understanding of their evolutionary origins and biogeographic history is limited as the sister lineage of notothenioids remains unidentified. The phylogenetic placement of notothenioids among major lineages of perciform fishes, which include sculpins, rockfishes, sticklebacks, eelpouts, scorpionfishes, perches, groupers and soapfishes, remains unresolved. We investigate the phylogenetic position of notothenioids using DNA sequences of 10 protein coding nuclear genes sampled from more than 650 percomorph species. The biogeographic history of notothenioids is reconstructed using a maximum likelihood method that integrates phylogenetic relationships, estimated divergence times, geographic distributions and paleogeographic history.ResultsPercophis brasiliensis is resolved, with strong node support, as the notothenioid sister lineage. The species is endemic to the subtropical and temperate Atlantic coast of southern South America. Biogeographic reconstructions imply the initial diversification of notothenioids involved the western portion of the East Gondwanan Weddellian Province. The geographic disjunctions among the major lineages of notothenioids show biogeographic and temporal correspondence with the fragmentation of East Gondwana.ConclusionsThe phylogenetic resolution of Percophis requires a change in the classification of percomorph fishes and provides evidence for a western Weddellian origin of notothenioids. The biogeographic reconstruction highlights the importance of the geographic and climatic isolation of Antarctica in driving the radiation of cold-adapted notothenioids.

Phylogeny and evolution of Indo-Pacific shrimp-associated gobies (Gobiiformes: Gobiidae)

Despite the ubiquity of obligate mutualisms on coral reef ecosystems, little is known about the evolution of many participating species. The shrimp gobies, known primarily from the coral reef habitats of the Indo-Pacific, are small benthic fishes that participate in a remarkable mutualism with alpheid shrimp. In this mutualism, the shrimp build and maintain a burrow that is guarded by the goby, and the shrimp and goby engage in an intricate tactile communication system. The mutualism is obligate for most shrimp gobies as participating species are highly vulnerable to predation when separated from a shrimp partner. We use phylogenetic analysis of nuclear and mitochondrial DNA sequence data to infer evolutionary relationships among shrimp gobies, and between shrimp gobies and their non-mutualistic gobiid relatives. We show that the mutualist shrimp association has arisen twice among gobies, once in a clade composed of Amblyeleotris, Ctenogobiops, and Vanderhorstia, and a second time in a clade including Cryptocentrus, Mahidolia, Tomiamichthys and Stonogobiops. We then compare the evolution of traits within each shrimp goby clade and consider their intrarelationships. We document cryptic diversity among shrimp gobies, with three distinct clades delineated among Mahidolia mysticina specimens captured at the same locality, paired with the same shrimp species. Mahidolia is placed as sister to the Cryptocentrus species Cryptocentrus cinctus; both exhibit pronounced dichromatism, occurring in both brown and yellow (xanthic) forms. We additionally clarify species identities within Amblyeleotris, confirming that widespread similar species Amblyeleotris fasciata, Amblyeleotris steinitzi and Amblyeleotris wheeleri are all distinct. We hypothesize that the flexibility of gobiid gobies and alpheid shrimp to interact with mutualist partners, as well as the apparently highly beneficial nature of mutualism between them, has contributed to the dual evolution of shrimp-association among Indo-Pacific gobies.