A phylogenomic framework for pelagiarian fishes (Acanthomorpha: Percomorpha) highlights mosaic radiation in the open ocean

Abstract

The fish clade Pelagiaria, which includes tunas as its most famous members, evolved remarkable morphological and ecological variety in a setting not generally considered conducive to diversification: the open ocean. Relationships within Pelagiaria have proven elusive due to short internodes subtending major lineages suggestive of rapid early divergences. Using a novel sequence dataset of over 1000 ultraconserved DNA elements (UCEs) for 94 of the 286 species of Pelagiaria (more than 70% of genera), we provide a time-calibrated phylogeny for this widely distributed clade. Some inferred relationships have clear precedents (e.g. the monophyly of 'core' Stromateoidei, and a clade comprising 'Gempylidae' and Trichiuridae), but others are unexpected despite strong support (e.g. Chiasmodontidae + Tetragonurus). Relaxed molecular clock analysis using node-based fossil calibrations estimates a latest Cretaceous origin for Pelagiaria, with crown-group families restricted to the Cenozoic. Estimated mean speciation rates decline from the origin of the group in the latest Cretaceous, although credible intervals for root and tip rates are broad and overlap in most cases, and there is higher-than-expected partitioning of body shape diversity (measured as fineness ratio) between clades concentrated during the Palaeocene-Eocene. By contrast, more direct measures of ecology show either no substantial deviation from a null model of diversification (diet) or patterns consistent with evolutionary constraint or high rates of recent change (depth habitat). Collectively, these results indicate a mosaic model of diversification. Pelagiarians show high morphological disparity and modest species richness compared to better-studied fish radiations in contrasting environments. However, this pattern is also apparent in other clades in open-ocean or deep-sea habitats, and suggests that comparative study of such groups might provide a more inclusive model of the evolution of diversity in fishes.

Keywords: UCE; adaptive radiation; pelagic realm; speciation; ultraconserved elements.

Figure 1.

Time-calibrated phylogeny of Pelagiaria based on topology inferred from 75% complete data matrix (1007 UCE loci). Statistical support values for nodes are indicated by monochrome shaded discs. Maximum likelihood bootstrap (ML) and Bayesian posterior probability (BPP) support are indicated by the left and right halves of the discs, respectively. Nodes without discs received support of 100% ML and 1.0 BPP. Red discs indicate the placement of fossil calibrations, with numerals corresponding to calibration numbers given in electronic supplementary material. Pampus argenteus, Ariomma indicum, Ruvettus pretiosus, Promethichthys prometheus: J. E. Randall (CC BY-NC); Peprilus burti: © R. Robertson (with permission); Ariomma bondi: © J. Kolding (with permission); Cubiceps whiteleggii: H. B. Osmany (CC BY-NC); Pomatomus saltatrix: NOAA; Icosteus aenigmaticus: J. P. Williams (CC BY-NC); Arripis trutta: Australian National Fish Collection/CISRO (CC BY-NC); Aphanopus carbo: © Pedro Niny Duarte/Universitário dos Açores (with permission). All other images from [41] (pls 144 B,G,E; 145 B; 217 D-E; 219 D-E; 220 F-G; 221 E; 223 E; 224 B,D,F-G; 233 A, G-E), © Tokai University Press, used with permission. See electronic supplementary material table S2 for further details.

Figure 2.

Patterns of evolutionary diversification in Pelagiaria. (a) BAMM-estimated mean speciation rates for 100 time-scaled phylogenies drawn from the posterior distribution of a topologically constrained BEAST divergence dating analysis (n = 100). Dashed vertical line indicates the K/Pg boundary. (b) Proportion of trees showing significant deviations from a subclade disparity through time (DTT) trajectory based on a constant rate Brownian motion null model for fineness ratio. Bar height at a given timestep indicates number of trees showing significant positive (above horizontal line) or negative (below horizontal line) deviations from the null. Grey envelope represents an accumulation curve, indicating the total number of trees showing at least one interval of significant deviation before that time. (c) Proportion of trees showing significant deviations from a subclade disparity through time (DTT) trajectory based on a constant rate Brownian motion null model for log₁₀ (mean depth). (d) Contour mapped [47] consensus of trees used in (a–c) showing evolution of fineness ratio. (e) Contour mapped consensus of trees used in (a–c) showing evolution of depth ecology. Differences between trees in (d) and (e) reflect differing availability of data for fineness ratio and depth ecology. Abbreviations: A., Arripidae; Bram., Bramidae; C., Caristiidae; Ce., Centrolophidae; Chia., Chiasmodontidae; I., Icosteidae; P., Pomatomidae; S., Scombrolabracidae; Scomb., Scombridae; Strom., ‘core’ Stromateoidei (Ariommatidae + Nomeidae + Stromateidae); T., Tetragonuridae; Trich.: Trichiuroidei (‘Gempylidae’ + Trichiuridae).