Prolonged morphological expansion of spiny-rayed fishes following the end-Cretaceous.

Spiny-rayed fishes (Acanthomorpha) dominate modern marine habitats and account for more than a quarter of all living vertebrate species. Previous time-calibrated phylogenies and patterns from the fossil record explain this dominance by correlating the origin of major acanthomorph lineages with the Cretaceous-Palaeogene mass extinction. Here we infer a time-calibrated phylogeny using ultraconserved elements that samples 91.4% of all acanthomorph families and investigate patterns of body shape disparity. Our results show that acanthomorph lineages steadily accumulated throughout the Cenozoic and underwent a significant expansion of among-clade morphological disparity several million years after the end-Cretaceous. These acanthomorph lineages radiated into and diversified within distinct regions of morphospace that characterize iconic lineages, including fast-swimming open-ocean predators, laterally compressed reef fishes, bottom-dwelling flatfishes, seahorses and pufferfishes. The evolutionary success of spiny-rayed fishes is the culmination of multiple species-rich and phenotypically disparate lineages independently diversifying across the globe under a wide range of ecological conditions.

Patterns of Phenotypic Evolution Associated with Marine/Freshwater Transitions in Fishes.

Evolutionary transitions between marine and freshwater ecosystems have occurred repeatedly throughout the phylogenetic history of fishes. The theory of ecological opportunity predicts that lineages that colonize species-poor regions will have greater potential for phenotypic diversification than lineages invading species-rich regions. Thus, transitions between marine and freshwaters may promote phenotypic diversification in trans-marine/freshwater fish clades. We used phylogenetic comparative methods to analyze body size data in nine major fish clades that have crossed the marine/freshwater boundary. We explored how habitat transitions, ecological opportunity, and community interactions influenced patterns of phenotypic diversity. Our analyses indicated that transitions between marine and freshwater habitats did not drive body size evolution, and there are few differences in body size between marine and freshwater lineages. We found that body size disparity in freshwater lineages is not correlated with the number of independent transitions to freshwaters. We found a positive correlation between body size disparity and overall species richness of a given area, and a negative correlation between body size disparity and diversity of closely related species. Our results indicate that the diversity of incumbent freshwater species does not restrict phenotypic diversification, but the diversity of closely related taxa can limit body size diversification. Ecological opportunity arising from colonization of novel habitats does not seem to have a major effect in the trajectory of body size evolution in trans-marine/freshwater clades. Moreover, competition with closely related taxa in freshwaters has a greater effect than competition with distantly related incumbent species.

Phylogeny, diversification, and biogeography of a hemiclonal hybrid system of native Australian freshwater fishes (Gobiiformes: Gobioidei: Eleotridae: Hypseleotris).

BACKGROUND: Carp gudgeons (genus Hypseleotris) are a prominent part of the Australian freshwater fish fauna, with species distributed around the western, northern, and eastern reaches of the continent. We infer a calibrated phylogeny of the genus based on nuclear ultraconserved element (UCE) sequences and using Bayesian estimation of divergence times, and use this phylogeny to investigate geographic patterns of diversification with GeoSSE. The southeastern species have hybridized to form hemiclonal lineages, and we also resolve relationships of hemiclones and compare their phylogenetic placement in the UCE phylogeny with a hypothesis based on complete mitochondrial genomes. We then use phased SNPs extracted from the UCE sequences for population structure analysis among the southeastern species and hemiclones. RESULTS: Hypseleotris cyprinoides, a widespread euryhaline species known from throughout the Indo-Pacific, is resolved outside the remainder of the species. Two Australian radiations comprise the bulk of Hypseleotris, one primarily in the northwestern coastal rivers and a second inhabiting the southeastern region including the Murray-Darling, Bulloo-Bancannia and Lake Eyre basins, plus coastal rivers east of the Great Dividing Range. Our phylogenetic results reveal cytonuclear discordance between the UCE and mitochondrial hypotheses, place hemiclone hybrids among their parental taxa, and indicate that the genus Kimberleyeleotris is nested within the northwestern Hypseleotris radiation along with three undescribed species. We infer a crown age for Hypseleotris of 17.3 Ma, date the radiation of Australian species at roughly 10.1 Ma, and recover the crown ages of the northwestern (excluding H. compressa) and southeastern radiations at 5.9 and 7.2 Ma, respectively. Range-dependent diversification analyses using GeoSSE indicate that speciation and extinction rates have been steady between the northwestern and southeastern Australian radiations and between smaller radiations of species in the Kimberley region and the Arnhem Plateau. Analysis of phased SNPs confirms inheritance patterns and reveals high levels of heterozygosity among the hemiclones. CONCLUSIONS: The northwestern species have restricted ranges and likely speciated in allopatry, while the southeastern species are known from much larger areas, consistent with peripatric speciation or allopatric speciation followed by secondary contact. Species in the northwestern Kimberley region differ in shape from those in the southeast, with the Kimberley species notably more elongate and slender than the stocky southeastern species, likely due to the different topographies and flow regimes of the rivers they inhabit.

Delayed Adaptive Radiation among New Zealand Stream Fishes: Joint Estimation of Divergence Time and Trait Evolution in a Newly Delineated Island Species Flock.

Adaptive radiations are generally thought to occur soon after a lineage invades a region offering high levels of ecological opportunity. However, few adaptive radiations beyond a handful of exceptional examples are known, so a comprehensive understanding of their dynamics is still lacking. Here, we present a novel case of an island species flock of freshwater fishes with a radically different tempo of adaptive history than that found in many popular evolutionary model systems. Using a phylogenomic data set combined with simultaneous Bayesian estimation of divergence times and trait-based speciation and extinction models, we show that the New Zealand Gobiomorphus gudgeons comprise a monophyletic assemblage, but surprisingly, the radiation did not fully occupy freshwater habitats and explosively speciate until more than 10 myr after the lineage invaded the islands. This shift in speciation rate was not accompanied by an acceleration in the rate of morphological evolution in the freshwater crown clade relative to the other species, but is correlated with a reduction in head pores and scales as well as an increase in egg size. Our results challenge the notion that clades always rapidly exploit ecological opportunities in the absence of competing lineages. Instead, we demonstrate that adaptive radiation can experience a slow start before undergoing accelerated diversification and that lineage and phenotypic diversification may be uncoupled in young radiations. [Adaptive radiation; Eleotridae; freshwater; Gobiomorphus; New Zealand.].

Supermatrix phylogeny resolves goby lineages and reveals unstable root of Gobiaria.

Gobies, sleepers, and cardinalfishes represent major clades of a species rich radiation of small bodied, ecologically diverse percomorphs (Gobiaria). Molecular phylogenetics has been crucial to resolving broad relationships of sleepers and gobies (Gobioidei), but the phylogenetic placements of cardinalfishes and nurseryfishes, as reciprocal or sequential sister clades to Gobioidei, are uncertain. In order to evaluate relationships among and within families we used a phylogenetic data mining approach to generate densely sampled trees inclusive of all higher taxa. We utilized conspecific amino acid homology to improve alignment accuracy, included ambiguously identified taxa to increase taxon sampling density, and resampled individual gene alignments to filter rogue sequences before concatenation. This approach yielded the most comprehensive tree yet of Gobiaria, inferred from a sparse (17 percent-complete) supermatrix of one ribosomal and 22 protein coding loci (18,065 characters), comprised of 50 outgroup and 777 ingroup taxa, representing 32 percent of species and 68 percent of genera. Our analyses confirmed the lineage-based classification of gobies with strong support, identified sleeper clades with unforeseen levels of systematic uncertainty, and quantified competing phylogenetic signals that confound resolution of the root topology. We also discovered that multilocus data completeness was related to maximum likelihood branch support, and verified that the phylogenetic uncertainty of shallow relationships observed within goby lineages could largely be explained by supermatrix sparseness. These results demonstrate the potential and limits of publicly available sequence data for producing densely-sampled phylogenetic trees of exceptionally biodiverse groups.

Temporal genetic analysis of the endangered tidewater goby: extinction-colonization dynamics or drift in isolation?

Extinction and colonization dynamics are critical to understanding the evolution and conservation of metapopulations. However, traditional field studies of extinction-colonization are potentially fraught with detection bias and have rarely been validated. Here, we provide a comparison of molecular and field-based approaches for assessment of the extinction-colonization dynamics of tidewater goby (Eucyclogobius newberryi) in northern California. Our analysis of temporal genetic variation across 14 northern California tidewater goby populations failed to recover genetic change expected with extinction-colonization cycles. Similarly, analysis of site occupancy data from field studies (94 sites) indicated that extinction and colonization are very infrequent for our study populations. Comparison of the approaches indicated field data were subject to imperfect detection, and falsely implied extinction-colonization cycles in several instances. For northern California populations of tidewater goby, we interpret the strong genetic differentiation between populations and high degree of within-site temporal stability as consistent with a model of drift in the absence of migration, at least over the past 20-30 years. Our findings show that tidewater goby exhibit different population structures across their geographic range (extinction-colonization dynamics in the south vs. drift in isolation in the north). For northern populations, natural dispersal is too infrequent to be considered a viable approach for recolonizing extirpated populations, suggesting that species recovery will likely depend on artificial translocation in this region. More broadly, this work illustrates that temporal genetic analysis can be used in combination with field data to strengthen inference of extinction-colonization dynamics or as a stand-alone tool when field data are lacking.

Rampant drift in artificially fragmented populations of the endangered tidewater goby (Eucyclogobius newberryi).

Habitat fragmentation and its genetic consequences are a critically important issue in evaluating the evolutionary penalties of human habitat modification. Here, we examine the genetic structure and diversity in naturally subdivided and artificially fragmented populations of the endangered tidewater goby (Eucyclogobius newberryi), a small fish restricted to discrete coastal lagoons and estuaries in California, USA. We use five naturally fragmented coastal populations from a 300- km spatial scale as a standard to assess migration and drift relative to eight artificially fragmented bay populations from a 30- km spatial scale. Using nine microsatellite loci in 621 individuals, and a 522-base fragment of mitochondrial DNA control region from 103 individuals, we found striking differences in the relative influences of migration and drift on genetic variation at these two scales. Overall, the artificially fragmented populations exhibited a consistent pattern of higher genetic differentiation and significantly lower genetic diversity relative to the naturally fragmented populations. Thus, even in a species characterized by habitat isolation and subdivision, further artificial fragmentation appears to result in substantial population genetic consequences and may not be sustainable.