Kristen L. Kuhn

Resolution of ray-finned fish phylogeny and timing of diversification

Ray-finned fishes make up half of all living vertebrate species. Nearly all ray-finned fishes are teleosts, which include most commercially important fish species, several model organisms for genomics and developmental biology, and the dominant component of marine and freshwater vertebrate faunas. Despite the economic and scientific importance of ray-finned fishes, the lack of a single comprehensive phylogeny with corresponding divergence-time estimates has limited our understanding of the evolution and diversification of this radiation. Our analyses, which use multiple nuclear gene sequences in conjunction with 36 fossil age constraints, result in a well-supported phylogeny of all major ray-finned fish lineages and molecular age estimates that are generally consistent with the fossil record. This phylogeny informs three long-standing problems: specifically identifying elopomorphs (eels and tarpons) as the sister lineage of all other teleosts, providing a unique hypothesis on the radiation of early euteleosts, and offering a promising strategy for resolution of the “bush at the top of the tree” that includes percomorphs and other spiny-finned teleosts. Contrasting our divergence time estimates with studies using a single nuclear gene or whole mitochondrial genomes, we find that the former underestimates ages of the oldest ray-finned fish divergences, but the latter dramatically overestimates ages for derived teleost lineages. Our time-calibrated phylogeny reveals that much of the diversification leading to extant groups of teleosts occurred between the late Mesozoic and early Cenozoic, identifying this period as the “Second Age of Fishes.”

Phylogeny and tempo of diversification in the superradiation of spiny-rayed fishes

Spiny-rayed fishes, or acanthomorphs, comprise nearly one-third of all living vertebrates. Despite their dominant role in aquatic ecosystems, the evolutionary history and tempo of acanthomorph diversification is poorly understood. We investigate the pattern of lineage diversification in acanthomorphs by using a well-resolved time-calibrated phylogeny inferred from a nuclear gene supermatrix that includes 520 acanthomorph species and 37 fossil age constraints. This phylogeny provides resolution for what has been classically referred to as the “bush at the top” of the teleost tree, and indicates acanthomorphs originated in the Early Cretaceous. Paleontological evidence suggests acanthomorphs exhibit a pulse of morphological diversification following the end Cretaceous mass extinction; however, the role of this event on the accumulation of living acanthomorph diversity remains unclear. Lineage diversification rates through time exhibit no shifts associated with the end Cretaceous mass extinction, but there is a global decrease in lineage diversification rates 50 Ma that occurs during a period when morphological disparity among fossil acanthomorphs increases sharply. Analysis of clade-specific shifts in diversification rates reveal that the hyperdiversity of living acanthomorphs is highlighted by several rapidly radiating lineages including tunas, gobies, blennies, snailfishes, and Afro-American cichlids. These lineages with high diversification rates are not associated with a single habitat type, such as coral reefs, indicating there is no single explanation for the success of acanthomorphs, as exceptional bouts of diversification have occurred across a wide array of marine and freshwater habitats.

Ancient climate change, antifreeze, and the evolutionary diversification of Antarctic fishes

The Southern Ocean around Antarctica is among the most rapidly warming regions on Earth, but has experienced episodic climate change during the past 40 million years. It remains unclear how ancient periods of climate change have shaped Antarctic biodiversity. The origin of antifreeze glycoproteins (AFGPs) in Antarctic notothenioid fishes has become a classic example of how the evolution of a key innovation in response to climate change can drive adaptive radiation. By using a time-calibrated molecular phylogeny of notothenioids and reconstructed paleoclimate, we demonstrate that the origin of AFGP occurred between 42 and 22 Ma, which includes a period of global cooling approximately 35 Ma. However, the most species-rich lineages diversified and evolved significant ecological differences at least 10 million years after the origin of AFGPs, during a second cooling event in the Late Miocene (11.6–5.3 Ma). This pattern indicates that AFGP was not the sole trigger of the notothenioid adaptive radiation. Instead, the bulk of the species richness and ecological diversity originated during the Late Miocene and into the Early Pliocene, a time coincident with the origin of polar conditions and increased ice activity in the Southern Ocean. Our results challenge the current understanding of the evolution of Antarctic notothenioids suggesting that the ecological opportunity that underlies this adaptive radiation is not linked to a single trait, but rather to a combination of freeze avoidance offered by AFGPs and subsequent exploitation of new habitats and open niches created by increased glacial and ice sheet activity.

Nuclear gene-inferred phylogenies resolve the relationships of the enigmatic Pygmy Sunfishes, Elassoma (Teleostei: Percomorpha).

Elassoma, the Pygmy Sunfishes, has long proven difficult to classify among the more than 15,000 species of percomorph fishes. Hypotheses dating to the 19th Century include Elassoma in Centrarchidae or in the monogeneric Elassomatidae, and more recent phylogenetic hypotheses have classified Elassoma in Smegmamorpha that also contained Synbranchiformes, Mugiliformes, Gasterosteiformes, and Atherinomorpha. No published phylogenetic analysis of morphological or molecular data has supported the monophyly of Smegmamorpha, or a consistent resolution of Elassoma relationships. In this study, we investigated the phylogenetic relationships of Elassoma and test the monophyly of Smegmamorpha with a nucleotide dataset comprising 10 protein-coding nuclear genes sampled from 65 percomorph species. Maximum likelihood analyses of each individual gene and the concatenated 10 genes all result in strong support for a clade composed of Elassoma and Centrarchidae, and no analysis supports monophyly of Smegmamorpha. Based on these results, a rank-free phylogenetic definition of Centrarchidae is presented that includes Elassoma, and the continued recognition of Smegmamorpha is discouraged. We discuss the implications of these phylogenetic analyses for relationships of several other percomorph lineages, including Kyphosidae, Terapontidae, Kuhliidae, Cheilodactylidae, Percichthyidae, Howellidae, Enoplosidae, Sinipercidae, and Cirrhitidae.

Phylogeny of Trematomus (Notothenioidei: Nototheniidae) inferred from mitochondrial and nuclear gene sequences

Abstract The biota of Antarctica is amazingly rich and highly endemic. The phylogenetics of notothenioid fishes has been extensively investigated through analyses of morphological characters, DNA sequences from mitochondrial genes, and single copy nuclear genes. These phylogenetic analyses have produced reasonably similar phylogenetic trees of notothenioids, however a number of phylogenetic questions remain. The nototheniid clade Trematomus is an example of a group where phylogenetic relationships remain unresolved. In this paper we revisit the phylogenetic relationships of Trematomus using both increased taxon sampling and an expanded dataset which includes DNA sequences from two mitochondrial genes (ND2 and 16S rRNA) and one single-copy nuclear gene (RPS7). The Bayesian phylogeny resulting from the analysis of the combined mitochondrial and nuclear gene datasets was well resolved and contained more interspecific nodes supported with significant Bayesian posteriors than either the mitochondrial or nuclear gene phylogenies alone. This demonstrates that the addition of nuclear gene sequence data to mitochondrial data can enhance phylogenetic resolution and increase node support. Additionally, the results of the combined mitochondrial and nuclear Bayesian analyses provide further support for the inclusion of species previously classified as Pagothenia and Cryothenia in Trematomus.

Biology of the Antarctic dragonfish Vomeridens infuscipinnis (Notothenioidei: Bathydraconidae)

Abstract Nineteen specimens of the rare dragonfish Vomeridens infuscipinnis were evaluated for meristic counts, morphometric measurements, vomerine teeth and the supratemporal canal, anatomical and histological observations of bone, cartilage and lipid, diet, and reproductive status. Seven individuals were measured for buoyancy. All specimens had small vomerine teeth that varied in number. There was also variability in the arrangement of the supratemporal pores and canals. Vomeridens possess a body with little bone and considerable amounts of cartilage and lipid. A mean percentage buoyancy of 1.61% indicated that Vomeridens is nearly neutrally buoyant. Inferences from measurements of buoyancy and from morphological data suggest that Vomeridens lives in an epibenthic water column habitat at 400–900 m. Facilitated by its reduced body density, Vomeridens are likely to forage in the water column by hovering above the substrate. The stomach contents consisted of krill (Euphausia superba), some as large as 46–50 mm.The absolute and relative fecundity in seven female was 1576–2296 oocytes (mean 1889) and 21.3–28.9 oocytes g-1 body weight (mean 25.3), respectively. The reproductive effort in terms of egg diameter, GSI, and absolute and relative fecundity is similar to that for other bathydraconids.

Aspects of the Biology and Population Genetics of the Antarctic Nototheniid Fish Trematomus nicolai

Abstract Trematomus nicolai is a near shore benthic notothenioid fish most abundant in the subzero shelf waters of East Antarctica. During recent collecting we obtained the first specimens of this species from West Antarctica (the Bransfield Strait), and we compare these with specimens from the Ross Sea (McMurdo Sound) in East Antarctica. Because T. nicolai has been frequently misidentified as T. tokarevi, we provide several non-meristic characters that separate these species. We employ a radiographic technique for rapid visualization of the cephalic lateral-line canals, an important diagnostic character in trematomids. Compared to those from McMurdo Sound, the Bransfield Strait specimens have lower ranges and mean counts for meristic characters, with significant differences for anal rays, pectoral rays, and vertebrae. Our data suggest a panmictic population, but the Bransfield Strait specimens live in water 3–4°C warmer than McMurdo Sound, and this may contribute to lower meristic counts. The mean buoyancy between the two samples is not significantly different. We examined sequence variation in the ND2 portion of the mitochondrial DNA (mtDNA) genome for evidence of population structure in samples from both areas. We identified 12 mtDNA haplotypes (haplotype diversity [h] = 0.978, nucleotide diversity [π] = 0.458%) and analysis of molecular variance (AMOVA) shows no significant global differentiation. A median-joining network that represents the genealogical relationships among the mitochondrial haplotypes also shows little separation between the samples from West and East Antarctica, and additional tests suggest the T. nicolai population is in equilibrium and of constant size. Trematomus nicolai exemplifies the potential of the Antarctic current regime for circum-Antarctic dispersal of a variety of organisms in the Southern Ocean.