Dahiana Arcila

The Tree of Life and a New Classification of Bony Fishes

The tree of life of fishes is in a state of flux because we still lack a comprehensive phylogeny that includes all major groups. The situation is most critical for a large clade of spiny-finned fishes, traditionally referred to as percomorphs, whose uncertain relationships have plagued ichthyologists for over a century. Most of what we know about the higher-level relationships among fish lineages has been based on morphology, but rapid influx of molecular studies is changing many established systematic concepts. We report a comprehensive molecular phylogeny for bony fishes that includes representatives of all major lineages. DNA sequence data for 21 molecular markers (one mitochondrial and 20 nuclear genes) were collected for 1410 bony fish taxa, plus four tetrapod species and two chondrichthyan outgroups (total 1416 terminals). Bony fish diversity is represented by 1093 genera, 369 families, and all traditionally recognized orders. The maximum likelihood tree provides unprecedented resolution and high bootstrap support for most backbone nodes, defining for the first time a global phylogeny of fishes. The general structure of the tree is in agreement with expectations from previous morphological and molecular studies, but significant new clades arise. Most interestingly, the high degree of uncertainty among percomorphs is now resolved into nine well-supported supraordinal groups. The order Perciformes, considered by many a polyphyletic taxonomic waste basket, is defined for the first time as a monophyletic group in the global phylogeny. A new classification that reflects our phylogenetic hypothesis is proposed to facilitate communication about the newly found structure of the tree of life of fishes. Finally, the molecular phylogeny is calibrated using 60 fossil constraints to produce a comprehensive time tree. The new time-calibrated phylogeny will provide the basis for and stimulate new comparative studies to better understand the evolution of the amazing diversity of fishes.

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.

Genome-wide interrogation advances resolution of recalcitrant groups in the tree of life

Much progress has been achieved in disentangling evolutionary relationships among species in the tree of life, but some taxonomic groups remain difficult to resolve despite increasing availability of genome-scale data sets. Here we present a practical approach to studying ancient divergences in the face of high levels of conflict, based on explicit gene genealogy interrogation (GGI). We show its efficacy in resolving the controversial relationships within the largest freshwater fish radiation (Otophysi) based on newly generated DNA sequences for 1,051 loci from 225 species. Initial results using a suite of standard methodologies revealed conflicting phylogenetic signal, which supports ten alternative evolutionary histories among early otophysan lineages. By contrast, GGI revealed that the vast majority of gene genealogies supports a single tree topology grounded on morphology that was not obtained by previous molecular studies. We also reanalysed published data sets for exemplary groups with recalcitrant resolution to assess the power of this approach. GGI supports the notion that ctenophores are the earliest-branching animal lineage, and adds insight into relationships within clades of yeasts, birds and mammals. GGI opens up a promising avenue to account for incompatible signals in large data sets and to discern between estimation error and actual biological conflict explaining gene tree discordance.

Molecular phylogeny of the subfamily Stevardiinae Gill, 1858 (Characiformes: Characidae): classification and the evolution of reproductive traits

BackgroundThe subfamily Stevardiinae is a diverse and widely distributed clade of freshwater fishes from South and Central America, commonly known as “tetras” (Characidae). The group was named “clade A” when first proposed as a monophyletic unit of Characidae and later designated as a subfamily. Stevardiinae includes 48 genera and around 310 valid species with many species presenting inseminating reproductive strategy. No global hypothesis of relationships is available for this group and currently many genera are listed as incertae sedis or are suspected to be non-monophyletic.ResultsWe present a molecular phylogeny with the largest number of stevardiine species analyzed so far, including 355 samples representing 153 putative species distributed in 32 genera, to test the group’s monophyly and internal relationships. The phylogeny was inferred using DNA sequence data from seven gene fragments (mtDNA: 12S, 16S and COI; nuclear: RAG1, RAG2, MYH6 and PTR). The results support the Stevardiinae as a monophyletic group and a detailed hypothesis of the internal relationships for this subfamily.ConclusionsA revised classification based on the molecular phylogeny is proposed that includes seven tribes and also defines monophyletic genera, including a resurrected genus Eretmobrycon, and new definitions for Diapoma, Hemibrycon, Bryconamericus sensu stricto, and Knodus sensu stricto, placing some small genera as junior synonyms. Inseminating species are distributed in several clades suggesting that reproductive strategy is evolutionarily labile in this group of fishes.

Comprehensive phylogeny of ray-finned fishes (Actinopterygii) based on transcriptomic and genomic data

Significance Ray-finned fishes form the largest and most diverse group of vertebrates. Establishing their phylogenetic relationships is a critical step to explaining their diversity. We compiled the largest comparative genomic database of fishes that provides genome-scale support for previous phylogenetic results and used it to resolve further some contentious relationships in fish phylogeny. A vetted set of exon markers identified in this study is a promising resource for current sequencing approaches to significantly increase genetic and taxonomic coverage to resolve the tree of life for all fishes. Our time-calibrated analysis suggests that most lineages of living fishes were already established in the Mesozoic Period, more than 65 million years ago. Our understanding of phylogenetic relationships among bony fishes has been transformed by analysis of a small number of genes, but uncertainty remains around critical nodes. Genome-scale inferences so far have sampled a limited number of taxa and genes. Here we leveraged 144 genomes and 159 transcriptomes to investigate fish evolution with an unparalleled scale of data: >0.5 Mb from 1,105 orthologous exon sequences from 303 species, representing 66 out of 72 ray-finned fish orders. We apply phylogenetic tests designed to trace the effect of whole-genome duplication events on gene trees and find paralogy-free loci using a bioinformatics approach. Genome-wide data support the structure of the fish phylogeny, and hypothesis-testing procedures appropriate for phylogenomic datasets using explicit gene genealogy interrogation settle some long-standing uncertainties, such as the branching order at the base of the teleosts and among early euteleosts, and the sister lineage to the acanthomorph and percomorph radiations. Comprehensive fossil calibrations date the origin of all major fish lineages before the end of the Cretaceous.

A new family of gymnodont fish (Tetraodontiformes) from the earliest Eocene of the Peri-Tethys (Kabardino-Balkaria, northern Caucasus, Russia)

The environmental changes that occurred during the Paleocene–Eocene transition are crucial for the interpretation of the patterns and processes of diversification of vertebrate clades. A prominent increase of the number of vertebrate families occurred between the late Paleocene and early Eocene, resulting in the appearance of many in the earliest representatives of extant lineages, including a number of marine fish groups. Tetraodontiforms are a monophyletic group of derived teleost fishes encompassing a variety of bizarre morphologies. Even though the earliest members of this order appeared in the Late Cretaceous, most of the crown lineages date back to the Eocene. One of the crown tetraodontiform groups that appeared in the fossil record during the Eocene are the gymnodonts (pufferfishes, porcupinefishes, ocean sunfishes and their allies), which include a variety of species characterized by highly modified teeth incorporated into beak-like jaws and scales usually modified into prickly spines. Herein, we describe †Balkaria histiopterygia gen. et sp. nov., a gymnodont fish characterized by a strikingly peculiar morphology. The single available specimen in part and counterpart documented herein was recovered from the sapropelitic deposits that originated in the northern Peri-Tethys during the transition between the Paleocene and Eocene. Today, these deposits are exposed near the village of Gerpegezh, Republic of Kabardino-Balkaria, Russia. The skeletal structure reveals an extreme mosaicism of primitive and derived characters that result in a very bizarre and unexpected morphology. †Balkaria histiopterygia gen. et sp. nov. is unique among the extant and other fossil gymnodont fishes by, among many other features, the huge size of its spiny-dorsal fin and the position of these spines on the top of the head. †Balkaria histiopterygia gen. et sp. nov. is the earliest unequivocal gymnodont fish, representing the sole member of the new family †Balkariidae. More particularly, †Balkaria histiopterygia gen. et sp. nov. is shown herein to be the oldest and arguably the most informative fossil of the gymnodont suborder Tetraodontoidei. The phylogenetic placement of this new taxon has been assessed based on both morphology alone and on a combination of morphological and molecular data that strongly supports the close relationship of †Balkaria gen. nov. to the herein restricted Tetraodontoidei. However, its position within Tetraodontoidei is unstable depending on the type of method of phylogenetic inference. Significantly younger ages, during the Late Cretaceous, are estimated for the diversification of Tetraodontiformes than in previous tip-dating analyses (Jurassic and Early Cretaceous) using the fossilized birth-death process; these new age estimates are in better agreement with the tetraodontiform fossil record. http://zoobank.org/urn:lsid:zoobank.org:pub:41764800-B0D8-4CA4-A111-5F4C4A281C37

Revision of the Neotropical Genus Acrobrycon (Ostariophysi: Characiformes: Characidae) with Description of Two New Species

Acrobrycon, a genus of Neotropical freshwater fishes from the western Amazon and northwestern portions of the La Plata basin is revised. The genus is found to include three species, two of which are new to science. Acrobrycon ipanquianus is distributed from the western portions of the Río Amazonas through to the northwestern region of the Río de La Plata basin; A. starnesi, new species, in the southwestern portion of the Amazon basin in Bolivia; and A. ortii, new species, in the northwestern Río de La Plata basin in Argentina. Members of the genus are distinguished from each other on the basis of the depth at the dorsal-fin origin, the horizontal eye diameter, the least interorbital width, and the numbers of perforated lateral-line scales, anal-fin rays, and horizontal scales around the caudal peduncle. The analysis found that A. tarijae, described from the Río Lipeo in Bolivia, cannot be distinguished morphologically from A. ipanquianus; thus, A. tarijae is placed into the synonymy of A. ipanquianus. En este estudio se revisan los caracidos neotropicales del género Acrobrycon. El género incluye tres especies, dos de las cuales son nuevas para la ciencia. Acrobrycon ipanquianus se distribuye desde la cuenca oriental del Río Amazonas hasta el noroccidente de la cuenca del Río de La Plata en Argentina; A. starnesi, especie nueva, ocurre en la porción suroccidental de la cuenca del Río Amazonas en Bolivia; A. ortii, especie nueva, esta restringida al noroccidente de la cuenca del Río de La Plata en Argentina. Los miembros de Acrobrycon se diferencian entre si con base en la profundidad del origen de la aleta dorsal, el diámetro horizontal del ojo, el ancho interobital, el numero de escamas perforadas en la línea lateral, el numero de radios en la aleta anal, y el numero de escamas horizontales alrededor del pedúnculo caudal. Este análisis indica Acrobrycon ipanquianus descrita para el Río Urubamba en Peru y A. tarijae, no pueden ser diferenciados morfologicamente y por ende A. tarijae se considera un sinónimo de A. ipanquianus.

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.

Trophic evolution in African citharinoid fishes (Teleostei: Characiformes) and the origin of intraordinal pterygophagy

The African freshwater suborder Citharinoidei (Characiformes) includes 110 species that exhibit a diversity of feeding modes comparable to those characteristic of more speciose groups such its sister, the Characoidei (2000+ species) or the distantly related Cichlidae (1600+ species). Feeding habits of the Citharinoidei range from generalist omnivores to highly specialized feeding modes including ectoparasitic fin-eating, i.e. pterygophagy. We examine diet preference evolution in the Citharinoidei using newly inferred multi-gene-based hypotheses of phylogenetic relationships for representatives of 12 of the 15 genera in the suborder. Ancestral character state reconstructions onto our best tree indicate that the three most-generalist diets - pelophage/planktivore, omnivore and invertivore - are also the most primitive conditions within the Citharinoidei. The feeding mode of the most recent common ancestor of the Citharinoidei was characterized by high uncertainty. The more specialized feeding habits - herbivory, piscivory and pterygophagy - originated later in the Citharinoidei, likely from invertivore ancestors and possibly across a short time period. Highly specialized fin eaters (Belonophago, Phago and Eugnatichthys) share a common origin along with a strict piscivore (Mesoborus) and an invertivore (Microstomatichthyoborus). The largely piscivorous, but facultative fin eater, Ichthyborus is not exclusively related to them. Our results demonstrate that overall diet preference transitions in the Citharinoidei were rare events with very few reversals or parallelisms, and that evolutionary shifts in trophic ecology have not played a major role in intraordinal diversification. This situation contrasts with other groups in which dietary transitions have played key roles in species diversification.