Laurie Sorenson

A Phylogenomic Perspective on the Radiation of Ray-Finned Fishes Based upon Targeted Sequencing of Ultraconserved Elements (UCEs).

Ray-finned fishes constitute the dominant radiation of vertebrates with over 32,000 species. Although molecular phylogenetics has begun to disentangle major evolutionary relationships within this vast section of the Tree of Life, there is no widely available approach for efficiently collecting phylogenomic data within fishes, leaving much of the enormous potential of massively parallel sequencing technologies for resolving major radiations in ray-finned fishes unrealized. Here, we provide a genomic perspective on longstanding questions regarding the diversification of major groups of ray-finned fishes through targeted enrichment of ultraconserved nuclear DNA elements (UCEs) and their flanking sequence. Our workflow efficiently and economically generates data sets that are orders of magnitude larger than those produced by traditional approaches and is well-suited to working with museum specimens. Analysis of the UCE data set recovers a well-supported phylogeny at both shallow and deep time-scales that supports a monophyletic relationship between Amia and Lepisosteus (Holostei) and reveals elopomorphs and then osteoglossomorphs to be the earliest diverging teleost lineages. Our approach additionally reveals that sequence capture of UCE regions and their flanking sequence offers enormous potential for resolving phylogenetic relationships within ray-finned fishes.

Iterative Ecological Radiation and Convergence during the Evolutionary History of Damselfishes (Pomacentridae)

Coral reef fishes represent one of the most spectacularly diverse assemblages of vertebrates on the planet, but our understanding of their mode of diversification remains limited. Here we test whether the diversity of the damselfishes (Pomacentridae), one of the most species-rich families of reef-associated fishes, was produced by a single or multiple adaptive radiation(s) during their evolutionary history. Tests of the tempo of lineage diversification using a time-calibrated phylogeny including 208 species revealed that crown pomacentrid diversification has not slowed through time as expected under a scenario of a single adaptive radiation resulting from an early burst of diversification. Evolutionary modeling of trophic traits similarly rejected the hypothesis of early among-lineage partitioning of ecologically important phenotypic diversity. Instead, damselfishes are shown to have experienced iterative convergent radiations wherein subclades radiate across similar trophic strategies (i.e., pelagic feeders, benthic feeders, intermediate) and morphologies. Regionalization of coral reefs, competition, and functional constraints may have fueled iterative ecological radiation and convergent evolution of damselfishes. Through the Pomacentridae, we illustrate that radiations may be strongly structured by the nature of the constraints on diversification.

The effect of habitat on modern shark diversification

Sharks occupy marine habitats ranging from shallow, inshore environments to pelagic, and deepwaters, and thus provide a model system for testing how gross habitat differences have shaped vertebrate macroevolution. Palaeontological studies have shown that onshore lineages diversify more quickly than offshore taxa. Among onshore habitats, coral reef‐association has been shown to increase speciation rates in several groups of fishes and invertebrates. In this study, we investigated whether speciation rates are habitat dependent by generating the first comprehensive molecular timescale for shark divergence. Using phylogenetic comparative methods, we rejected the hypothesis that shelf (i.e. onshore) lineages have higher speciation rates compared to those occupying deepwater and oceanic (i.e. offshore) habitats. Our results, however, support the hypothesis of increased speciation rates in coral reef‐associated lineages within the Carcharhinidae. Our new timetree suggests that the two major shark lineages leading to the extant shark diversity began diversifying mostly after the end‐Permian mass extinction: the squalimorphs into deepwater and the galeomorphs into shelf habitats. We suggest that the breakdown of the onshore–offshore speciation rate pattern in sharks is mediated by success in deepwater environments through ecological partitioning, and in some cases, the evolution of morphological novelty.

A multi-locus timetree of surgeonfishes (Acanthuridae, Percomorpha), with revised family taxonomy

We present the most comprehensive time-calibrated, species-level hypothesis of the timing of Acanthuridae (surgeonfishes and allies) evolution based on 76% of the extant diversity and nine genes. We recover two major acanthurid clades, Nasinae and Acanthurinae, and infer a much more recent Nasinae crown age (17 Ma) compared to a previous dating study for Naso. The Acanthurinae represent an older group that originated ~42 Ma, with most diversification occurring since the Early Miocene (beginning ~21 Ma). Our results strongly support a paraphyletic Acanthurus and Ctenochaetus, with multiple analyses recovering a clade grouping Ctenochaetus, A. nubilus and A. pyroferus. Contrary to previous studies, we also provide strong evidence that thick-walled, gizzard-like stomachs evolved only once within Acanthurus and that this morphology has a common origin in Acanthurus and Ctenochaetus. Based on our molecular analyses, in conjunction with the large body of morphological evidence, we recommend dissolving the genus Ctenochaetus into the genus Acanthurus.

A new multi-locus timescale reveals the evolutionary basis of diversity patterns in triggerfishes and filefishes (Balistidae, Monacanthidae; Tetraodontiformes)

Balistoid fishes (triggerfishes, filefishes, leatherjackets) represent one of the most successful radiations of tetraodontiform fishes across the worlds oceans. Balistids (triggerfishes) are largely circumtropical in coral reef environments while most monacanthids (filefishes, leatherjackets) are distributed across reef and non-reef habitats in the Indo-western Pacific. Although members of these clades share a distinctive mode of locomotion that relies upon coordinated oscillation or undulation of enlarged dorsal and anal fins, species richness as well as morphologial and ecological diversity are generally considered to be higher in monacanthids than in triggerfishes. Explicit evolutionary comparisons of diversity patterns between these sister clades have been hampered by the paucity of systematic studies of filefishes relative to triggerfishes. Furthermore, a well-sampled molecular timescale for balistoids is lacking, hindering our understanding of the evolutionary history of these fishes. Here, we produce the largest balistoid molecular dataset to date, based on two mitochondrial and three nuclear loci, for a total of 86 species, and we time-calibrate it using three tetraodontiform fossils. We show that several of the traditional monacanthid genera are not monophyletic and that the balistid Xenobalistes tumidipectoris is nested within the genus Xanthichthys, and suggest that the generic name Xenobalistes be dissolved. Our timetree reveals a Late Miocene origin of balistids, in accordance with previous studies, but a Late Eocene age for the crown monacanthids, which experienced significant diversification during the Late Oligocene and Early Miocene. Comparative analyses reveal no significant family-level differences in rates of speciation or body size evolution, suggesting that the greater diversity of filefishes can be attributed to their more ancient crown age compared to triggerfishes.

A new phylogeny of tetraodontiform fishes (Tetraodontiformes, Acanthomorpha) based on 22 loci.

Tetraodontiform fishes represent one of the most peculiar radiations of teleost fishes. In spite of this, we do not currently have a consensus on the phylogenetic relationships among the major tetraodontiform lineages, with different morphological and molecular datasets all supporting contrasting relationships. In this paper we present the results of the analysis of tetraodontiform interrelationships based on two mitochondrial and 20 nuclear loci for 40 species of tetraodontiforms (representing all of the 10 currently recognized families), as well as three outgroups. Bayesian and maximum likelihood analyses of the concatenated dataset (18,682 nucleotides) strongly support novel relationships among the major tetraodontiform lineages. Our results recover two large clades already found in mitogenomic analyses (although the position of triacanthids differ), while they strongly conflict with hypotheses of tetraodontiform relationships inferred by previous studies based on morphology, as well as studies of higher-level teleost relationships based on nuclear loci, which included multiple tetraodontiform lineages. A parsimony gene-tree, species-tree analysis recovers relationships that are mostly congruent with the analyses of the concatenated dataset, with the significant exception of the position of the pufferfishes+porcupine fishes clade. Our findings suggest that while the phylogenetic placement of some tetraodontiform lineages (triacanthids, molids) remains problematic even after sequencing 22 loci, an overall molecular consensus is beginning to emerge regarding the existence of several major clades. This new hypothesis will require a re-evaluation of the phylogenetic usefulness of several morphological features, such as the fusion of several jaw bones into a parrot-like beak, or the reduction and loss of some of the fins, which may have occurred independently more times than previously thought.

A multilocus molecular phylogeny of boxfishes (Aracanidae, Ostraciidae; Tetraodontiformes).

Boxfishes (superfamily Ostracioidea, order Tetraodontiformes) are comprised of 37 species within the families Aracanidae (13 sp.) and Ostracidae (24 sp.). These species are characterized by several dramatic reductive trends in their axial and appendicular skeleton, and by the presence of a carapace formed by enlarged and thickened scale plates. While strong support exists for the monophyly of both families, interspecific relationships remain unclear as no species-level molecular phylogeny currently exists for either of these two clades, and the only hypotheses of relationships are based on morphological studies that were mostly restricted to generic-level relationships. Here we present the results of a new phylogenetic study of a dataset composed of 9 loci for 26 species of boxfishes using both likelihood and Bayesian methods. Our topology strongly supports the monophyly of both groups, and additionally provides strongly supported resolution for the vast majority of species-level interrelationships. Based on this new phylogeny, we suggest changing the taxonomic status of the species Lactoria fornasini to Tetrasomus fornasini, and Rhynchostracion nasus to Ostracion nasus. Using a Bayesian approach to divergence time estimation we inferred a Paleocene origin of the Ostracioidea, with an estimated origin of the reef-associated ostraciids spanning the Eocene and Oligocene, and a Miocene/Pliocene origin of the aracanids.

First molecular scombrid timetree (Percomorpha: Scombridae) shows recent radiation of tunas following invasion of pelagic habitat

Abstract Scombrid fishes represent one of the major radiations of marine vertebrates in the pelagic realm, and have historically been a commercially important group. Their rich fossil record dates to the Late Paleocene, and it has recently been suggested that the current scombrid diversity is due to a post-Cretaceous radiation that saw the survivors of the KPg extinction replace a number of non-acanthomorph fish lineages that did not survive the Mesozoic Era. In this paper we present the result of the first quantitative macroevolutionary study of scombrid evolution. We assembled a supermatrix consisting of seven nuclear and mitochondrial loci, including 47 of the 52 extant scombrid species. We then used seven fossils to time-calibrate this new molecular phylogeny, the first ever assembled for scombrids that included more than 50% of the diversity of this family, and investigated macroevolutionary patterns within this clade. Our results support a Late Cretaceous origin of the scombrids, and show that many lineages originated in the Eocene and Oligocene. Our findings, however, fail to support the hypothesis of a rapid scombrid radiation in the post-KPg ecosystems. We show how the most significant radiation within scombrids has taken place since the Late Miocene in tunas, possibly triggered by a transition from pelagic-neritic to pelagic-oceanic habitats, and matched by a dramatic increase in body size.

Evolutionary patterns of adaptive acrobatics and physical performance predict expression profiles of androgen receptor – but not oestrogen receptor – in the forelimb musculature

1. Superior physical competence is vital to the adaptive behavioral routines of many animals, particularly those that engage in elaborate socio-sexual displays. How such traits evolve across species remains unclear. 2. Recent work suggests that activation of sex steroid receptors in neuromuscular systems is necessary for the fine motor skills needed to execute physically elaborate displays. Thus, using passerine birds as models, we test whether interspecific variation in display complexity predicts species differences in the abundance of androgen and estrogen receptors (AR and ERα) expressed in the forelimb musculature and spinal cord. 3. We find that small-scale evolutionary patterns in physical display complexity positively predict expression of the AR in the main muscles that lift and retract the wings. No such relationship is detected in the spinal cord, and we do not find a correlation between display behavior and neuromuscular expression of ERα. Also, we find that AR expression levels in different androgen targets throughout the body - namely the wing muscles, spinal cord, and testes - are not necessarily correlated, providing evidence that evolutionary forces may drive AR expression in a tissue-specific manner. 4. These results suggest co-evolution between the physical prowess necessary for display performance and levels of AR expression in avian forelimb muscles. Moreover, this relationship appears to be specific to muscle and AR-mediated, but not ERα-mediated, signaling. 5. Given that prior work suggests that activation of muscular AR is a necessary component of physical display performance, our current data support the hypothesis that sexual selection shapes levels of AR expressed in the forelimb skeletal muscles to help drive the evolution of adaptive motor abilities.

First multi-locus timetree of seabreams and porgies (Percomorpha: Sparidae)

Abstract Sparid fishes represent one of the major radiations of predominantly temperate-water benthic fishes. Previous molecular phylogenetic studies suggested that many traditional taxonomic groups, often based on dentition characters, do not correspond to monophyletic groups, suggesting repeated convergence in trophic ecology. In spite of the rich sparid fossil record, no comprehensive, multi-locus timetree based on sparid fossils currently exists for this group. We used a supermatrix approach to assemble a dataset of five loci and 91 sparid species, and time-calibrated this new phylogeny using eight sparid fossils. Our study corroborates the non-monophyly of the traditional sparids without the inclusion of the family Centracanthidae, as well as that of many sparid genera. Based on phylogenetic comparative analyses we find robust support for a scenario of multiple radiations and suggest that these were driven by the invasion of multiple geographic regions by different lineages, as well as by the transition to different trophic ecologies.