The impact of paleoclimatic changes on body size evolution in marine fishes.

Body size is an important species trait, correlating with life span, fecundity, and other ecological factors. Over Earth's geological history, climate shifts have occurred, potentially shaping body size evolution in many clades. General rules attempting to summarize body size evolution include Bergmann's rule, which states that species reach larger sizes in cooler environments and smaller sizes in warmer environments, and Cope's rule, which poses that lineages tend to increase in size over evolutionary time. Tetraodontiform fishes (including pufferfishes, boxfishes, and ocean sunfishes) provide an extraordinary clade to test these rules in ectotherms owing to their exemplary fossil record and the great disparity in body size observed among extant and fossil species. We examined Bergmann's and Cope's rules in this group by combining phylogenomic data (1,103 exon loci from 185 extant species) with 210 anatomical characters coded from both fossil and extant species. We aggregated data layers on paleoclimate and body size from the species examined, and inferred a set of time-calibrated phylogenies using tip-dating approaches for downstream comparative analyses of body size evolution by implementing models that incorporate paleoclimatic information. We found strong support for a temperature-driven model in which increasing body size over time is correlated with decreasing oceanic temperatures. On average, extant tetraodontiforms are two to three times larger than their fossil counterparts, which otherwise evolved during periods of warmer ocean temperatures. These results provide strong support for both Bergmann's and Cope's rules, trends that are less studied in marine fishes compared to terrestrial vertebrates and marine invertebrates.

Evolutionary Dynamics of the OR Gene Repertoire in Teleost Fishes: Evidence of an Association with Changes in Olfactory Epithelium Shape.

Teleost fishes perceive their environment through a range of sensory modalities, among which olfaction often plays an important role. Richness of the olfactory repertoire depends on the diversity of receptors coded by homologous genes classified into four families: OR, TAAR, VR1, and VR2. Herein, we focus on the OR gene repertoire. While independent large contractions of the OR gene repertoire associated with ecological transitions have been found in mammals, little is known about the diversity of the OR gene repertoire and its evolution in teleost fishes, a group that includes more than 34,000 living species. We analyzed genomes of 163 species representing diversity in this large group. We found a large range of variation in the number of functional OR genes, from 15 in the Broad-nose Pipefish Syngnathus typhle and the Ocean Sunfish Mola mola, to 429 in the Zig-zag Eel Mastacembelus armatus. The number of OR genes was higher in species when a multilamellar olfactory rosette was present. Moreover, the number of lamellae was correlated with the richness of the OR gene repertoire. While a slow and balanced birth-and-death process generally drives the evolution of the OR gene repertoire, we inferred several episodes of high rates of gene loss, sometimes followed by large gains in the number of OR genes. These gains coincide with morphological changes of the olfactory organ and suggest a strong functional association between changes in the morphology and the evolution of the OR gene repertoire.

Review of the Indian Ocean spikefish genus Mephisto (Tetraodontiformes: Triacanthodidae).

We redescribe the triacanthodid spikefish Mephisto fraserbrunneri Tyler 1966 based upon eight specimens (five newly reported herein) and the first color photographs of freshly collected specimens; these data are compared with that of the single specimen of the recently described M. albomaculosus Matsuura, Psomadakis, and Mya Than Tun 2018. Both species are found in the Indian Ocean, with M. fraserbrunneri known from the Arabian Sea off the east coast of Africa to the eastern Bay of Bengal, and M. albomaculosus confirmed only from the type locality in the Andaman Sea (a color photograph of an individual M. cf. albomaculosus from the Bay of Bengal that was not retained is also presented). We describe and diagnose the genus Mephisto and provide a key to the two species based upon all available specimens. We also provide a distribution map for both species and summarize literature records. Using micro-CT data, we show that Mephisto fraserbrunneri replaces teeth intraosseously, which suggests this tooth replacement pattern is plesiomorphic for Tetraodontiformes.

Life history, distribution and molecular phylogenetics of the Upward-Mouth Spikefish Atrophacanthus japonicus (Teleostei: Tetraodontiformes: Triacanthodidae).

Ninety-six juvenile specimens (37-54 mm standard length; LS ) of the rarely collected Upward-Mouth Spikefish Atrophacanthus japonicus (Triacanthodidae) were obtained from the stomachs of three Yellowfin Tuna Thunnus albacares collected off Guam in the Mariana Islands in the central Pacific Ocean. These specimens extend the range of A. japonicus eastward into Oceania. We review the systematic characters of the monotypic genus Atrophacanthus and present colour photographs of freshly collected specimens. The diet of the juvenile specimens of A. japonicus consisted of thecosome pteropods and foraminiferans. We present a range map of A. japonicus based on all known specimens and show that specimen size is related to whether specimens were collected in the pelagic zone or on the bottom. Our results support that, compared to all other Triacanthodidae, A. japonicus has an unusually extended pelagic larval and juvenile period, up to 54 mm LS , before settling to the bottom as adults. Lastly, we provide a multilocus phylogeny addressing the phylogenetic placement of Atrophacanthus based on eight of 11 triacanthodid genera and six genetic markers. Our results reveal that Atrophacanthus is the sister group of Macrorhamphosodes and they provide new insights about the evolutionary history of the family.

Mass extinction in tetraodontiform fishes linked to the Palaeocene-Eocene thermal maximum.

Integrative evolutionary analyses based upon fossil and extant species provide a powerful approach for understanding past diversification events and for assessing the tempo of evolution across the Tree of Life. Herein, we demonstrate the importance of integrating fossil and extant species for inferring patterns of lineage diversification that would otherwise be masked in analyses that examine only one source of evidence. We infer the phylogeny and macroevolutionary history of the Tetraodontiformes (triggerfishes, pufferfishes and allies), a group with one of the most extensive fossil records among fishes. Our analyses combine molecular and morphological data, based on an expanded matrix that adds newly coded fossil species and character states. Beyond confidently resolving the relationships and divergence times of tetraodontiforms, our diversification analyses detect a major mass-extinction event during the Palaeocene-Eocene Thermal Maximum (PETM), followed by a marked increase in speciation rates. This pattern is consistently obtained when fossil and extant species are integrated, whereas examination of the fossil occurrences alone failed to detect major diversification changes during the PETM. When taking into account non-homogeneous models, our analyses also detect a rapid lineage diversification increase in one of the groups (tetraodontoids) during the middle Miocene, which is considered a key period in the evolution of reef fishes associated with trophic changes and ecological opportunity. In summary, our analyses show distinct diversification dynamics estimated from phylogenies and the fossil record, suggesting that different episodes shaped the evolution of tetraodontiforms during the Cenozoic.

An evaluation of fossil tip-dating versus node-age calibrations in tetraodontiform fishes (Teleostei: Percomorphaceae).

Time-calibrated phylogenies based on molecular data provide a framework for comparative studies. Calibration methods to combine fossil information with molecular phylogenies are, however, under active development, often generating disagreement about the best way to incorporate paleontological data into these analyses. This study provides an empirical comparison of the most widely used approach based on node-dating priors for relaxed clocks implemented in the programs BEAST and MrBayes, with two recently proposed improvements: one using a new fossilized birth-death process model for node dating (implemented in the program DPPDiv), and the other using a total-evidence or tip-dating method (implemented in MrBayes and BEAST). These methods are applied herein to tetraodontiform fishes, a diverse group of living and extinct taxa that features one of the most extensive fossil records among teleosts. Previous estimates of time-calibrated phylogenies of tetraodontiforms using node-dating methods reported disparate estimates for their age of origin, ranging from the late Jurassic to the early Paleocene (ca. 150-59Ma). We analyzed a comprehensive dataset with 16 loci and 210 morphological characters, including 131 taxa (95 extant and 36 fossil species) representing all families of fossil and extant tetraodontiforms, under different molecular clock calibration approaches. Results from node-dating methods produced consistently younger ages than the tip-dating approaches. The older ages inferred by tip dating imply an unlikely early-late Jurassic (ca. 185-119Ma) origin for this order and the existence of extended ghost lineages in their fossil record. Node-based methods, by contrast, produce time estimates that are more consistent with the stratigraphic record, suggesting a late Cretaceous (ca. 86-96Ma) origin. We show that the precision of clade age estimates using tip dating increases with the number of fossils analyzed and with the proximity of fossil taxa to the node under assessment. This study suggests that current implementations of tip dating may overestimate ages of divergence in calibrated phylogenies. It also provides a comprehensive phylogenetic framework for tetraodontiform systematics and future comparative studies.

The importance of even highly incomplete fossil taxa in reconstructing the phylogenetic relationships of the tetraodontiformes (acanthomorpha: pisces).

The use of fossils in the phylogenetics of extant clades traditionally has been a contentious issue. Fossils usually are relatively incomplete, and their use commonly leads to an increase in the number of equally most parsimonious trees and a decrease in the resolution of phylogenies. Fossils alone, however, provide certain kinds of information about the biological history of a clade, and computer simulations have shown that even highly incomplete material can, under certain circumstances, increase the accuracy of a phylogeny, rather than decrease it.Because empirical data are still scarce on the effects of the inclusion of fossils on phylogenetic reconstructions, we attempted to investigate this problem by using a relatively well-known group of acanthomorph fishes, the Tetraodontiformes (triggerfishes, pufferfishes, and ocean sunfishes), for which robust phylogenies using extant taxa already exist and that has a well-studied fossil record. Adding incomplete fossil taxa of tetraodontiforms usually increases the number of equally most parsimonious trees and often decreases the resolution of consensus trees. However, adding fossil taxa may help to correctly establish relationships among lineages that have experienced high degrees of morphological diversification by allowing for a reinterpretation of homologous and homoplastic features, increasing the resolution rather than decreasing it. Furthermore, taxa that were scored for 25% or more of their characters did not cause a significant loss of resolution, while providing unique biological information.