Publications by authors named "Ricardo Betancur-R"

35 Publications

Deep reefs are not refugium for shallow-water fish communities in the southwestern Atlantic.

Ecol Evol 2021 May 18;11(9):4413-4427. Epub 2021 Mar 18.

Departamento de Sistemática e Ecologia Centro de Ciências Exatas e da Natureza Universidade Federal da Paraíba João Pessoa PB Brazil.

The deep reef refugia hypothesis (DRRH) predicts that deep reef ecosystems may act as refugium for the biota of disturbed shallow waters. Because deep reefs are among the most understudied habitats on Earth, formal tests of the DRRH remain scarce. If the DRRH is valid at the community level, the diversity of species, functions, and lineages of fish communities of shallow reefs should be encapsulated in deep reefs.We tested the DRRH by assessing the taxonomic, functional, and phylogenetic diversity of 22 Brazilian fish communities between 2 and 62 m depth. We partitioned the gamma diversity of shallow (<30 m) and deep reefs (>30 m) into independent alpha and beta components, accounted for species' abundance, and assessed whether beta patterns were mostly driven by spatial turnover or nestedness.We recorded 3,821 fishes belonging to 85 species and 36 families. Contrary to DRRH expectations, only 48% of the species occurred in both shallow and deep reefs. Alpha diversity of rare species was higher in deep reefs as expected, but alpha diversity of typical and dominant species did not vary with depth. Alpha functional diversity was higher in deep reefs only for rare and typical species, but not for dominant species. Alpha phylogenetic diversity was consistently higher in deep reefs, supporting DRRH expectations.Profiles of taxonomic, functional, and phylogenetic beta diversity indicated that deep reefs were not more heterogeneous than shallow reefs, contradicting expectations of biotic homogenization near sea surface. Furthermore, pairwise beta-diversity analyses revealed that the patterns were mostly driven by spatial turnover rather than nestedness at any depth. . Although some results support the DRRH, most indicate that the shallow-water reef fish diversity is not fully encapsulated in deep reefs. Every reef contributes significantly to the regional diversity and must be managed and protected accordingly.
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http://dx.doi.org/10.1002/ece3.7336DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8093723PMC
May 2021

Testing the utility of alternative metrics of branch support to address the ancient evolutionary radiation of tunas, stromateoids, and allies (Teleostei: Pelagiaria).

Syst Biol 2021 Mar 30. Epub 2021 Mar 30.

Department of Biology, University of Oklahoma, Norman, Oklahoma, U.S.A.

The use of high-throughput sequencing technologies to produce genome-scale datasets was expected to settle some long-standing controversies across the Tree of Life, particularly in areas where short branches occur at deep timescales. Instead, these datasets have often yielded many well-supported but conflicting topologies, and highly variable gene-tree distributions. A variety of branch-support metrics beyond the nonparametric bootstrap are now available to assess how robust a phylogenetic hypothesis may be, as well as new methods to quantify gene-tree discordance. We applied multiple branch support metrics to an ancient group of marine fishes (Teleostei: Pelagiaria) whose interfamilial relationships have proven difficult to resolve due to a rapid accumulation of lineages very early in its history. We analyzed hundreds of loci including published UCE data and newly generated exonic data along with their flanking regions to represent all 16 extant families for more than 150 out of 284 valid species in the group. Branch support was lower for interfamilial relationships (except the SH-like aLRT and aBayes methods) regardless of the type of marker used. Several nodes that were highly supported with bootstrap had very low site and gene-tree concordance, revealing underlying conflict. Despite this conflict, we were able to identify four consistent interfamilial clades, each comprised of two or three families. Combining exons with their flanking regions also produced increased branch lengths in the deep branches of the pelagiarian tree. Our results demonstrate the limitations of employing current metrics of branch support and species-tree estimation when assessing the confidence of ancient evolutionary radiations and emphasize the necessity to embrace alternative measurements to explore phylogenetic uncertainty and discordance in phylogenomic datasets.
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http://dx.doi.org/10.1093/sysbio/syab018DOI Listing
March 2021

Evolutionary determinism and convergence associated with water-column transitions in marine fishes.

Proc Natl Acad Sci U S A 2020 12 16;117(52):33396-33403. Epub 2020 Dec 16.

Department of Biology, The University of Oklahoma, Norman, OK 73019;

Repeatable, convergent outcomes are prima facie evidence for determinism in evolutionary processes. Among fishes, well-known examples include microevolutionary habitat transitions into the water column, where freshwater populations (e.g., sticklebacks, cichlids, and whitefishes) recurrently diverge toward slender-bodied pelagic forms and deep-bodied benthic forms. However, the consequences of such processes at deeper macroevolutionary scales in the marine environment are less clear. We applied a phylogenomics-based integrative, comparative approach to test hypotheses about the scope and strength of convergence in a marine fish clade with a worldwide distribution (snappers and fusiliers, family Lutjanidae) featuring multiple water-column transitions over the past 45 million years. We collected genome-wide exon data for 110 (∼80%) species in the group and aggregated data layers for body shape, habitat occupancy, geographic distribution, and paleontological and geological information. We also implemented approaches using genomic subsets to account for phylogenetic uncertainty in comparative analyses. Our results show independent incursions into the water column by ancestral benthic lineages in all major oceanic basins. These evolutionary transitions are persistently associated with convergent phenotypes, where deep-bodied benthic forms with truncate caudal fins repeatedly evolve into slender midwater species with furcate caudal fins. Lineage diversification and transition dynamics vary asymmetrically between habitats, with benthic lineages diversifying faster and colonizing midwater habitats more often than the reverse. Convergent ecological and functional phenotypes along the benthic-pelagic axis are pervasive among different lineages and across vastly different evolutionary scales, achieving predictable high-fitness solutions for similar environmental challenges, ultimately demonstrating strong determinism in fish body-shape evolution.
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http://dx.doi.org/10.1073/pnas.2006511117DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7777220PMC
December 2020

Exon probe sets and bioinformatics pipelines for all levels of fish phylogenomics.

Mol Ecol Resour 2021 Apr 21;21(3):816-833. Epub 2020 Nov 21.

Department of Biology, University of Oklahoma, Norman, OK, USA.

Exon markers have a long history of use in phylogenetics of ray-finned fishes, the most diverse clade of vertebrates with more than 35,000 species. As the number of published genomes increases, it has become easier to test exons and other genetic markers for signals of ancient duplication events and filter out paralogues that can mislead phylogenetic analysis. We present seven new probe sets for current target-capture phylogenomic protocols that capture 1,104 exons explicitly filtered for paralogues using gene trees. These seven probe sets span the diversity of teleost fishes, including four sets that target five hyperdiverse percomorph clades which together comprise ca. 17,000 species (Carangaria, Ovalentaria, Eupercaria, and Syngnatharia + Pelagiaria combined). We additionally included probes to capture legacy nuclear exons and mitochondrial markers that have been commonly used in fish phylogenetics (despite some exons being flagged for paralogues) to facilitate integration of old and new molecular phylogenetic matrices. We tested these probes experimentally for 56 fish species (eight species per probe set) and merged new exon-capture sequence data into an existing data matrix of 1,104 exons and 300 ray-finned fish species. We provide an optimized bioinformatics pipeline to assemble exon capture data from raw reads to alignments for downstream analysis. We show that legacy loci with known paralogues are at risk of assembling duplicated sequences with target-capture, but we also assembled many useful orthologous sequences that can be integrated with many PCR-generated matrices. These probe sets are a valuable resource for advancing fish phylogenomics because targeted exons can easily be extracted from increasingly available whole genome and transcriptome data sets, and also may be integrated with existing PCR-based exon and mitochondrial data.
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http://dx.doi.org/10.1111/1755-0998.13287DOI Listing
April 2021

New insights about species delimitation in red snappers (Lutjanus purpureus and L. campechanus) using multilocus data.

Mol Phylogenet Evol 2020 06 2;147:106780. Epub 2020 Mar 2.

Laboratório de Genética Aplicada, Instituto de Estudos Costeiros, Universidade Federal do Pará, Bragança, Pará, Brazil; Laboratório de Genética e Biologia Molecular, Instituto de Estudos Costeiros, Universidade Federal do Pará, Bragança, Pará, Brazil. Electronic address:

Lutjanus campechanus and Lutjanus purpureus are two commercially important lutjanid fishes (snappers) with non-sympatric distribution throughout Western Atlantic. Even though both taxa have traditionally been regarded as valid species, their taxonomic status remains under debate. In the present study, we used phylogeographic approaches and molecular methods of species delimitation to elucidate the taxonomic issues between both species, based on 1478 base pairs from four genomic regions. We found haplotypes shared between the two species, particularly in relation to nuclear DNA (nuDNA) sequences. The molecular delimitation of species supported the discrimination of L. purpureus and L. campechanus as distinct evolutionary units. Nonetheless, a unidirectional gene flow was found from L. campechanus towards L. purpureus. Therefore, it seems plausible to infer that L. campechanus and L. purpureus are two evolutionary units in which the apparent sharing of haplotypes should be driven by introgression.
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http://dx.doi.org/10.1016/j.ympev.2020.106780DOI Listing
June 2020

Biogeography, habitat transitions and hybridization in a radiation of South American silverside fishes revealed by mitochondrial and genomic RAD data.

Mol Ecol 2020 02 29;29(4):738-751. Epub 2020 Jan 29.

Department of Biological Sciences, George Washington University, Washington, DC, USA.

Rivers and lake systems in the southern cone of South America have been widely influenced by historical glaciations, carrying important implications for the evolution of aquatic organisms, including prompting transitions between marine and freshwater habitats and by triggering hybridization among incipient species via waterway connectivity and stream capture events. Silverside fishes (Odontesthes) in the region comprise a radiation of 19 marine and freshwater species that have been hypothesized on the basis of morphological or mitochondrial DNA data to have either transitioned repeatedly into continental waters from the sea or colonized marine habitats following freshwater diversification. New double digest restriction-site associated DNA data presented here provide a robust framework to investigate the biogeographical history of and habitat transitions in Odontesthes. We show that Odontesthes silversides originally diversified in the Pacific but independently colonized the Atlantic three times, producing three independent marine-to-freshwater transitions. Our results also indicate recent introgression of marine mitochondrial haplotypes into two freshwater clades, with more recurring instances of hybridization among Atlantic- versus Pacific-slope species. In Pacific freshwater drainages, hybridization with a marine species appears to be geographically isolated and may be related to glaciation events. Substantial structural differences of estuarine gradients between these two geographical areas may have influenced the frequency, intensity and evolutionary effects of hybridization events.
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http://dx.doi.org/10.1111/mec.15350DOI Listing
February 2020

On trends and patterns in macroevolution: Williston's law and the branchiostegal series of extant and extinct osteichthyans.

BMC Evol Biol 2019 06 10;19(1):117. Epub 2019 Jun 10.

CR2P, UMR 7207 (CNRS/MNHN/Sorbonne Université), Muséum National d'Histoire Naturelle, Bâtiment de Géologie, Case postale 48, 43 rue Buffon, F-75231, cedex 05, Paris, France.

Background: The branchiostegal series consists of an alignment of bony elements in the posterior portion of the skull of osteichthyan vertebrates. We trace the evolution of the number of elements in a comprehensive survey that includes 440 extant and 66 extinct species. Using a newly updated actinopterygian tree in combination with phylogenetic comparative analyses, we test whether osteichthyan branchiostegals follow an evolutionary trend under 'Williston's law', which postulates that osteichthyan lineages experienced a reduction of bony elements over time.

Results: We detected no overall macroevolutionary trend in branchiostegal numbers, providing no support for 'Williston's law'. This result is robust to the subsampling of palaeontological data, but the estimation of the model parameters is much more ambiguous.

Conclusions: We find substantial evidence for a macroevolutionary dynamic favouring an 'early burst' of trait evolution over alternative models. Our study highlights the challenges of accurately reconstructing macroevolutionary dynamics even with large amounts of data about extant and extinct taxa.
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http://dx.doi.org/10.1186/s12862-019-1436-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6558815PMC
June 2019

Post-Cretaceous bursts of evolution along the benthic-pelagic axis in marine fishes.

Proc Biol Sci 2018 Dec;285(1893):20182010

1 Department of Biology, University of Puerto Rico , Rio Piedras, PO Box 23360, San Juan, Puerto Rico 00931 , USA.

Ecological opportunity arising in the aftermath of mass extinction events is thought to be a powerful driver of evolutionary radiations. Here, we assessed how the wake of the Cretaceous-Palaeogene (K-Pg) mass extinction shaped diversification dynamics in a clade of mostly marine fishes (Carangaria), which comprises a disparate array of benthic and pelagic dwellers including some of the most astonishing fish forms (e.g. flatfishes, billfishes, remoras, archerfishes). Analyses of lineage diversification show time-heterogeneous rates of lineage diversification in carangarians, with highest rates reached during the Palaeocene. Likewise, a remarkable proportion of Carangaria's morphological variation originated early in the history of the group and in tandem with a marked incidence of habitat shifts. Taken together, these results suggest that all major lineages and body plans in Carangaria originated in an early burst shortly after the K-Pg mass extinction, which ultimately allowed the occupation of newly released niches along the benthic-pelagic habitat axis.
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http://dx.doi.org/10.1098/rspb.2018.2010DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6304066PMC
December 2018

Genomics overrules mitochondrial DNA, siding with morphology on a controversial case of species delimitation.

Proc Biol Sci 2019 04;286(1900):20182924

14 Department of Biology, The University of Oklahoma , 730 Van Vleet Oval, Room 314, Norman, OK 73019 , USA.

Species delimitation is a major quest in biology and is essential for adequate management of the organismal diversity. A challenging example comprises the fish species of red snappers in the Western Atlantic. Red snappers have been traditionally recognized as two separate species based on morphology: Lutjanus campechanus (northern red snapper) and L. purpureus (southern red snapper). Recent genetic studies using mitochondrial markers, however, failed to delineate these nominal species, leading to the current lumping of the northern and southern populations into a single species ( L. campechanus). This decision carries broad implications for conservation and management as red snappers have been commercially over-exploited across the Western Atlantic and are currently listed as vulnerable. To address this conflict, we examine genome-wide data collected throughout the range of the two species. Population genomics, phylogenetic and coalescent analyses favour the existence of two independent evolutionary lineages, a result that confirms the morphology-based delimitation scenario in agreement with conventional taxonomy. Despite finding evidence of introgression in geographically neighbouring populations in northern South America, our genomic analyses strongly support isolation and differentiation of these species, suggesting that the northern and southern red snappers should be treated as distinct taxonomic entities.
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http://dx.doi.org/10.1098/rspb.2018.2924DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6501682PMC
April 2019

Chinchaysuyoa, a new genus of the fish family Ariidae (Siluriformes), with a redescription of Chinchaysuyoa labiata from Ecuador and a new species description from Peru.

Zootaxa 2019 Jan 31;4551(3):361-378. Epub 2019 Jan 31.

Laboratorio de Biologia e Genética de Peixes, Instituto de Biociências, UNESP, 18618-689, Botucatu, SP, Brazil.

In recent years, morphological and molecular studies have improved our understanding about the relationships and classification schemes of the marine catfishes of the family Ariidae. A taxonomic issue that is still contentious concerns the limits and status of the freshwater Neotropical ariid diversity, in particular the species in the genus Potamarius. The delimitation of Potamarius is currently uncertain given the disjunct distribution of the species in Mesoamerica (Potamarius izabalensis, P. nelsoni and P. usumacintae, from Lake Izabal and Usumacinta River basins in Mexico to Guatemala) and Brazil (P. grandoculis, from coastal lakes in southeastern Brazil). The freshwater Arius labiatus and Hexanematichthys henni from the Peripa and Daule rivers in Ecuador that drain to the Eastern Pacific (EP), have also at times been listed as species inquirenda in Potamarius. Here, we redescribe Arius labiatus, redefine the taxonomic status of Hexanematichthys henni, as junior synonym of Arius labiatus, and describe a new species from Peru that is closely related to Arius labiatus. Based on morphological and molecular phylogenetic evidence, we also describe a new genus (Chinchaysuyoa) for the two South American species.
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http://dx.doi.org/10.11646/zootaxa.4551.3.5DOI Listing
January 2019

Comparative phylogeography of trans-Andean freshwater fishes based on genome-wide nuclear and mitochondrial markers.

Mol Ecol 2019 03;28(5):1096-1115

Laboratorio de Ictiología, Unidad de Ecología y Sistemática (UNESIS), Departamento de Biología, Facultad de Ciencias, Pontificia Universidad Javeriana, Bogotá, Colombia.

The Neotropical region represents one of the greatest biodiversity hot spots on earth. Despite its unparalleled biodiversity, regional comparative phylogeographic studies are still scarce, with most focusing on model clades (e.g. birds) and typically examining a handful of loci. Here, we apply a genome-wide comparative phylogeographic approach to test hypotheses of codiversification of freshwater fishes in the trans-Andean region. Using target capture methods, we examined exon data for over 1,000 loci combined with complete mitochondrial genomes to study the phylogeographic history of five primary fish species (>150 individuals) collected from eight major river basins in Northwestern South America and Lower Central America. To assess their patterns of genetic structure, we inferred genealogical concordance taking into account all major aspects of phylogeography (within loci, across multiple genes, across species and among biogeographic provinces). Based on phylogeographic concordance factors, we tested four a priori biogeographic hypotheses, finding support for three of them and uncovering a novel, unexpected pattern of codiversification. The four emerging inter-riverine patterns are as follows: (a) Tuira + Atrato, (b) Ranchería + Catatumbo, (c) Magdalena system and (d) Sinú + Atrato. These patterns are interpreted as shared responses to the complex uplifting and orogenic processes that modified or sundered watersheds, allowing codiversification and speciation over geological time. We also find evidence of cryptic speciation in one of the species examined and instances of mitochondrial introgression in others. These results help further our knowledge of the historical geographic factors shaping the outstanding biodiversity of the Neotropics.
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http://dx.doi.org/10.1111/mec.15036DOI Listing
March 2019

Phylogenomic incongruence, hypothesis testing, and taxonomic sampling: The monophyly of characiform fishes.

Evolution 2019 02 4;73(2):329-345. Epub 2018 Dec 4.

Department of Vertebrate Zoology, National Museum of Natural History Smithsonian Institution, Washington, DC, 20013.

Phylogenomic studies using genome-wide datasets are quickly becoming the state of the art for systematics and comparative studies, but in many cases, they result in strongly supported incongruent results. The extent to which this conflict is real depends on different sources of error potentially affecting big datasets (assembly, stochastic, and systematic error). Here, we apply a recently developed methodology (GGI or gene genealogy interrogation) and data curation to new and published datasets with more than 1000 exons, 500 ultraconserved element (UCE) loci, and transcriptomic sequences that support incongruent hypotheses. The contentious non-monophyly of the order Characiformes proposed by two studies is shown to be a spurious outcome induced by sample contamination in the transcriptomic dataset and an ambiguous result due to poor taxonomic sampling in the UCE dataset. By exploring the effects of number of taxa and loci used for analysis, we show that the power of GGI to discriminate among competing hypotheses is diminished by limited taxonomic sampling, but not equally sensitive to gene sampling. Taken together, our results reinforce the notion that merely increasing the number of genetic loci for a few representative taxa is not a robust strategy to advance phylogenetic knowledge of recalcitrant groups. We leverage the expanded exon capture dataset generated here for Characiformes (206 species in 23 out of 24 families) to produce a comprehensive phylogeny and a revised classification of the order.
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http://dx.doi.org/10.1111/evo.13649DOI Listing
February 2019

Mitochondrial genomes of the headstanders (Steindachner 1900) and (Valenciennes 1837), (Characiformes, Anostomidae).

Mitochondrial DNA B Resour 2018 May 23;3(2):634-636. Epub 2018 May 23.

Laboratorio de Ictiología, Unidad de Ecología y Sistemática -UNESIS-, Departamento de Biología, Facultad de Ciencias, Pontificia Universidad Javeriana, Bogotá, Colombia.

We report two mitochondrial genomes of headstanders, derived from target capture and Illumina sequencing (HiSeq 2500 PE100). One trans-Andean species (mitochondrial consensus genome of 25 individuals) from Colombia and one cis-Andean species from Argentina. Regarding , mitochondrial genome has 13 protein-coding genes, 1 D-loop, 2 ribosomal RNAs, 21 transfer RNAs, and is 14,434 bp in length, for mitochondrial genome has 13 protein-coding genes, 2 ribosomal RNAs, 22 transfer RNAs, and is 15,546 bp in length.
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http://dx.doi.org/10.1080/23802359.2018.1473723DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7800840PMC
May 2018

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

Proc Natl Acad Sci U S A 2018 06 14;115(24):6249-6254. Epub 2018 May 14.

Shenzhen Key Lab of Marine Genomics, Guangdong Provincial Key Lab of Molecular Breeding in Marine Economic Animals, Beijing Genomics Institute Academy of Marine Sciences, Beijing Genomics Institute Marine, Beijing Genomics Institute, 518083 Shenzhen, China;

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.
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http://dx.doi.org/10.1073/pnas.1719358115DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6004478PMC
June 2018

Mitochondrial genomes of the South American electric knifefishes (Steindachner 1878), (Schreiner and Miranda Ribeiro 1903), (Humboldt 1805) and (Bloch and Schneider 1801), (Gymnotiformes, Sternopygidae).

Mitochondrial DNA B Resour 2018 May 11;3(2):572-574. Epub 2018 May 11.

Laboratorio de Ictiología, Unidad de Ecología y Sistemática -Unesis, Departamento de Biología, Facultad de Ciencias Pontificia, Universidad Javeriana, Bogotá, Colombia.

We report four mitochondrial genomes of South American electric knifefishes, derived from target capture and Illumina sequencing (HiSeq 2500 PE100). Two trans-Andean species (mitochondrial consensus genome of 25 individuals) and (mitochondrial consensus genome of 30 individuals) from Colombia and two cis-Andean species from Suriname and from Argentina. Regarding , and mitochondrial genomes have 13 protein-coding genes, 1 D-loop, 2 ribosomal RNAs, 22 transfer RNAs, and are 13,394 bp, 10,921 bp, and 13,013 bp in length respectively, for mitochondrial genomes have 13 protein-coding genes, 2 ribosomal RNAs, 22 transfer RNAs, and is 14,270 bp in length.
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http://dx.doi.org/10.1080/23802359.2018.1469386DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7800563PMC
May 2018

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

Nat Ecol Evol 2017 Jan 13;1(2):20. Epub 2017 Jan 13.

Department of Vertebrate Zoology, National Museum of Natural History Smithsonian Institution, PO Box 37012, MRC 159, Washington DC 20013, USA.

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.
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http://dx.doi.org/10.1038/s41559-016-0020DOI Listing
January 2017

Phylogenetic classification of bony fishes.

BMC Evol Biol 2017 07 6;17(1):162. Epub 2017 Jul 6.

Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, DC, USA.

Background: Fish classifications, as those of most other taxonomic groups, are being transformed drastically as new molecular phylogenies provide support for natural groups that were unanticipated by previous studies. A brief review of the main criteria used by ichthyologists to define their classifications during the last 50 years, however, reveals slow progress towards using an explicit phylogenetic framework. Instead, the trend has been to rely, in varying degrees, on deep-rooted anatomical concepts and authority, often mixing taxa with explicit phylogenetic support with arbitrary groupings. Two leading sources in ichthyology frequently used for fish classifications (JS Nelson's volumes of Fishes of the World and W. Eschmeyer's Catalog of Fishes) fail to adopt a global phylogenetic framework despite much recent progress made towards the resolution of the fish Tree of Life. The first explicit phylogenetic classification of bony fishes was published in 2013, based on a comprehensive molecular phylogeny ( www.deepfin.org ). We here update the first version of that classification by incorporating the most recent phylogenetic results.

Results: The updated classification presented here is based on phylogenies inferred using molecular and genomic data for nearly 2000 fishes. A total of 72 orders (and 79 suborders) are recognized in this version, compared with 66 orders in version 1. The phylogeny resolves placement of 410 families, or ~80% of the total of 514 families of bony fishes currently recognized. The ordinal status of 30 percomorph families included in this study, however, remains uncertain (incertae sedis in the series Carangaria, Ovalentaria, or Eupercaria). Comments to support taxonomic decisions and comparisons with conflicting taxonomic groups proposed by others are presented. We also highlight cases were morphological support exist for the groups being classified.

Conclusions: This version of the phylogenetic classification of bony fishes is substantially improved, providing resolution for more taxa than previous versions, based on more densely sampled phylogenetic trees. The classification presented in this study represents, unlike any other, the most up-to-date hypothesis of the Tree of Life of fishes.
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http://dx.doi.org/10.1186/s12862-017-0958-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5501477PMC
July 2017

Widespread ecomorphological convergence in multiple fish families spanning the marine-freshwater interface.

Proc Biol Sci 2017 May;284(1854)

Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, PO Box 37012, MRC 159, Washington, DC 20013-7012, USA.

The theoretical definition and quantification of convergence is an increasingly topical focus in evolutionary research, with particular growing interest on study scales spanning deep phylogenetic divergences and broad geographical areas. While much progress has recently been made in understanding the role of convergence in driving terrestrial (e.g. anole lizards) and aquatic (e.g. cichlids) radiations, little is known about its macroevolutionary effects across environmental gradients. This study uses a suite of recently developed comparative approaches integrating diverse aspects of morphology, dietary data, habitat affiliation and phylogeny to assess convergence across several well-known tropical-temperate fish families in the percomorph suborder Terapontoidei, a clade with considerable phenotypic and ecological diversity radiating in both marine and freshwater environments. We demonstrate significant widespread convergence across many lineages occupying equivalent trophic niches, particularly feeding habits such as herbivory and biting of attached prey off hard substrates. These include several examples of convergent morphotypes evolving independently in marine and freshwater clades, separated by deep evolutionary divergences (tens of millions of years). The Terapontoidei present a new example of the macroevolutionary dynamics of morphological and ecological coevolution in relation to habitat and trophic preferences, at a greater phylogenetic and habitat scale than most well-studied adaptive radiations.
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http://dx.doi.org/10.1098/rspb.2017.0565DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5443956PMC
May 2017

Cathorops festae (Boulenger 1898) (Siluriformes; Ariidae), a valid species from Ecuador and Peru.

Zootaxa 2016 Sep 22;4170(1):137-148. Epub 2016 Sep 22.

Department of Biology, University of Puerto Rico, Río Piedras, P.O. Box 23360, San Juan 00931, Puerto Rico.; Email: unknown.

Over the past decade, the Sea Catfish (Ariidae) genus Cathorops has been the focus of a major taxonomic review, which has resulted in the revalidation of five synonymized nominal species, and the recognition of seven new species. With 21 valid species, Cathorops is currently the most species-rich genus of Ariidae in the New World. The principal lacuna in the taxonomic knowledge of genus species is the uncertain status of Arius festae Boulenger, 1898, described from Naranjal, in the Guayas River basin of Ecuador. In the present study Cathorops festae is redescribed as a valid species based on morphological and molecular data.
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http://dx.doi.org/10.11646/zootaxa.4170.1.7DOI Listing
September 2016

Herbivory Promotes Dental Disparification and Macroevolutionary Dynamics in Grunters (Teleostei: Terapontidae), a Freshwater Adaptive Radiation.

Am Nat 2016 Mar 22;187(3):320-33. Epub 2016 Jan 22.

Trophic shifts into new adaptive zones have played major (although often conflicting) roles in reshaping the evolutionary trajectories of many lineages. We analyze data on diet, tooth, and oral morphology and relate these traits to phenotypic disparification and lineage diversification rates across the ecologically diverse Terapontidae, a family of Australasian fishes. In contrast to carnivores and most omnivores, which have retained relatively simple, ancestral caniniform tooth shapes, herbivorous terapontids appear to have evolved a variety of novel tooth shapes at significantly faster rates to meet the demands of plant-based diets. The evolution of herbivory prompted major disparification, significantly expanding the terapontid adaptive phenotypic continuum into an entirely novel functional morphospace. There was minimal support for our hypothesis of faster overall rates of integrated tooth shape, spacing, and jaw biomechanical evolution in herbivorous terapontids in their entirety, compared with other trophic strategies. There was, however, considerable support for accelerated disparification within a diverse freshwater clade containing a range of specialized freshwater herbivores. While the evolutionary transition to herbivorous diets has played a central role in terapontid phenotypic diversification by pushing herbivores toward novel fitness peaks, there was little support for herbivory driving significantly higher lineage diversification compared with background rates across the family.
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http://dx.doi.org/10.1086/684747DOI Listing
March 2016

Phylogenetic placement of enigmatic percomorph families (Teleostei: Percomorphaceae).

Mol Phylogenet Evol 2016 Jan 19;94(Pt B):565-576. Epub 2015 Oct 19.

Department of Biology, University of Puerto Rico - Río Piedras, P.O. Box 23360, San Juan 00931, Puerto Rico. Electronic address:

Percomorphs are a large and diverse group of spiny-finned fishes that have come to be known as the "bush at the top" due to their persistent lack of phylogenetic resolution. Recently, the broader Euteleost Tree of Life project (EToL) inferred a well-supported phylogenetic hypothesis that groups the diversity of percomorphs into nine well-supported series (supraordinal groups): Ophidiaria, Batrachoidaria, Gobiaria, Syngnatharia, Pelagiaria, Anabantaria, Carangaria, Ovalentaria, and Eupercaria. The EToL also provided, for the first time, a monophyletic definition of Perciformes - the largest order of vertebrates. Despite significant progress made in accommodating the diversity of percomorph taxa into major clades, some 62 families (most previously placed in "Perciformes", as traditionally defined) were not examined by the EToL. Here, we provide evidence for the phylogenetic affinities of 10 of those 62 families, seven of which have largely remained enigmatic. This expanded taxonomic sampling also provides further support for the nine EToL supraordinal series. We examined sequences from 21 genes previously used by the EToL and added two fast-evolving mitochondrial markers in an attempt to increase resolution within the rapid percomorph radiations. We restricted the taxonomic sampling to 1229 percomorph species, including expanded sampling from recent studies. Results of maximum likelihood analysis revealed that bathyclupeids (Bathyclupeidae), galjoen fishes (Dichistiidae), kelpfishes (Chironemidae), marblefishes (Aplodactylidae), trumpeters (Latridae), barbeled grunters (Hapalogenyidae), slopefishes (Symphysanodontidae), and picarel porgies (formerly Centracanthidae) are members of the series Eupercaria ("new bush at the top"). The picarel porgies and porgies (Sparidae) are now placed in the same family (Sparidae). Our analyses suggest a close affinity between the orders Spariformes (including Lethrinidae, Nemipteridae and Sparidae) and Lobotiformes (including the tripletails or Lobotidae, the barbeled grunters, and tigerperches or Datnioididae), albeit support for this group is low. None of the newly examined families belong in the order Perciformes, as recently defined. Finally, we confirm results from other recent studies that place the Australasian salmons (Arripidae) within Pelagiaria, and the false trevallies (Lactariidae) close to flatfishes, jacks, and trevallies, within Carangaria.
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http://dx.doi.org/10.1016/j.ympev.2015.10.006DOI Listing
January 2016

Fossil-based comparative analyses reveal ancient marine ancestry erased by extinction in ray-finned fishes.

Ecol Lett 2015 May 23;18(5):441-50. Epub 2015 Mar 23.

Department of Biology, University of Puerto Rico - Río Piedras, P.O. Box 23360, San Juan, Puerto Rico, 00931; Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, PO Box 37012, Washington, DC, 20013, USA.

The marine-freshwater boundary is a major biodiversity gradient and few groups have colonised both systems successfully. Fishes have transitioned between habitats repeatedly, diversifying in rivers, lakes and oceans over evolutionary time. However, their history of habitat colonisation and diversification is unclear based on available fossil and phylogenetic data. We estimate ancestral habitats and diversification and transition rates using a large-scale phylogeny of extant fish taxa and one containing a massive number of extinct species. Extant-only phylogenetic analyses indicate freshwater ancestry, but inclusion of fossils reveal strong evidence of marine ancestry in lineages now restricted to freshwaters. Diversification and colonisation dynamics vary asymmetrically between habitats, as marine lineages colonise and flourish in rivers more frequently than the reverse. Our study highlights the importance of including fossils in comparative analyses, showing that freshwaters have played a role as refuges for ancient fish lineages, a signal erased by extinction in extant-only phylogenies.
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http://dx.doi.org/10.1111/ele.12423DOI Listing
May 2015

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

Mol Phylogenet Evol 2015 Jan 24;82 Pt A:131-45. Epub 2014 Oct 24.

Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, P.O. Box 37012, MRC 159, Washington, DC 20013, United States; Department of Biology, University of Puerto Rico - Río Piedras, P.O. Box 23360, San Juan 00931, Puerto Rico.

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.
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http://dx.doi.org/10.1016/j.ympev.2014.10.011DOI Listing
January 2015

A time-calibrated, multi-locus phylogeny of piranhas and pacus (Characiformes: Serrasalmidae) and a comparison of species tree methods.

Mol Phylogenet Evol 2014 Dec 28;81:242-57. Epub 2014 Sep 28.

Department of Biological Sciences, The George Washington University, 2023 G St. NW, Washington, DC 20052, USA. Electronic address:

The phylogeny of piranhas, pacus, and relatives (family Serrasalmidae) was inferred on the basis of DNA sequences from eleven gene fragments that include the mitochondrial control region plus 10 nuclear genes (two exons and eight introns). The new data were obtained for a representative sampling of 53 specimens, collected from all major South American rivers, accounting for over 40% of the valid species and all genera excluding Utiaritichthys. Two fossil calibration points and relaxed-clock Bayesian analyses were used to estimate the timing of diversification. The new multilocus dataset also is used to compare several species-tree approaches against the results obtained using the concatenated alignment analyzed under maximum likelihood and Bayesian inference. Individual gene trees showed substantial topological discordance, but analyses based on concatenation and Bayesian and maximum likelihood-based species trees approaches converged onto a single phylogeny. The resulting phylogenetic hypothesis is robust and supports a division of the family into three major clades, consistent with previous results based on mitochondrial DNA alone. The earliest branching event separated a "pacu" clade (Colossoma, Mylossoma and Piaractus) from the rest of the family in the Late Cretaceous (over 68 Ma). The other two clades, that contain most of the diversity, are formed by the "true piranhas" (Metynnis, Pygopristis, Pygocentrus, Pristobrycon, Catoprion, and Serrasalmus) and the Myleus-like pacus (the Myleus clade). The "true" piranha clade originated during the Eocene (∼53 Ma) but the most recent diversification of flesh-eating piranhas within the genera Serrasalmus and Pygocentrus did not start until the Miocene (∼17 Ma). A comparison of species tree approaches indicates that most methods tested are consistent with results obtained by concatenation, suggesting that the gene-tree incongruence observed is mild and will not produce misleading results under simple concatenation analysis. Non-monophyly of several genera (Pristobrycon, Tometes, Myloplus, Mylesinus) and putative species (Serrasalmus rhombeus) was obtained, suggesting that further study of this family is necessary.
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http://dx.doi.org/10.1016/j.ympev.2014.06.018DOI Listing
December 2014

Molecular evidence for the monophyly of flatfishes (Carangimorpharia: Pleuronectiformes).

Mol Phylogenet Evol 2014 Apr 18;73:18-22. Epub 2014 Jan 18.

Department of Biological Sciences, The George Washington University, 2023 G St. NW, Washington, DC 20052, United States. Electronic address:

Proliferation of phylogenetic studies based on poor taxonomic sampling or insufficient molecular evidence usually leads to conflicting results. As a consequence, advancement of systematic knowledge yields to confusion. The problem is exacerbated for taxonomic groups with historically difficult resolution of evolutionary relationships such as the flatfishes. Molecular evidence to support monophyly for this emblematic group of fishes and their interrelationships has been elusive, and a recent paper published in this journal went as far as to claim that flatfish monophyly can be rejected with molecular data, implying that the asymmetric body plan unique to these fishes had two independent origins. A reanalysis of this evidence suggests the contrary and combination of the new data with existing datasets unequivocally supports the monophyly of this group based on analyses of concatenated data as well as species tree approaches. Resolution of difficult phylogenetic problems requires analysis of larger datasets with adequate taxonomic coverage and sound hypothesis-testing procedures. Proliferation of partial studies claiming extraordinary results should be avoided in order to advance the field of molecular phylogenetics.
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http://dx.doi.org/10.1016/j.ympev.2014.01.006DOI Listing
April 2014

Conserved genes, sampling error, and phylogenomic inference.

Syst Biol 2014 Mar 30;63(2):257-62. Epub 2013 Nov 30.

Department of Biological Sciences, The George Washington University, 2023 G St. NW, Washington, DC 20052, USA; and College of Charleston, Hollings Marine Lab, 331 Fort Johnson Rd., Charleston, SC 29412, USA.

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http://dx.doi.org/10.1093/sysbio/syt073DOI Listing
March 2014

Multi-locus phylogenetic analysis reveals the pattern and tempo of bony fish evolution.

PLoS Curr 2013 Apr 16;5. Epub 2013 Apr 16.

University of Oklahoma.

Over half of all vertebrates are "fishes", which exhibit enormous diversity in morphology, physiology, behavior, reproductive biology, and ecology. Investigation of fundamental areas of vertebrate biology depend critically on a robust phylogeny of fishes, yet evolutionary relationships among the major actinopterygian and sarcopterygian lineages have not been conclusively resolved. Although a consensus phylogeny of teleosts has been emerging recently, it has been based on analyses of various subsets of actinopterygian taxa, but not on a full sample of all bony fishes. Here we conducted a comprehensive phylogenetic study on a broad taxonomic sample of 61 actinopterygian and sarcopterygian lineages (with a chondrichthyan outgroup) using a molecular data set of 21 independent loci. These data yielded a resolved phylogenetic hypothesis for extant Osteichthyes, including 1) reciprocally monophyletic Sarcopterygii and Actinopterygii, as currently understood, with polypteriforms as the first diverging lineage within Actinopterygii; 2) a monophyletic group containing gars and bowfin (= Holostei) as sister group to teleosts; and 3) the earliest diverging lineage among teleosts being Elopomorpha, rather than Osteoglossomorpha. Relaxed-clock dating analysis employing a set of 24 newly applied fossil calibrations reveals divergence times that are more consistent with paleontological estimates than previous studies. Establishing a new phylogenetic pattern with accurate divergence dates for bony fishes illustrates several areas where the fossil record is incomplete and provides critical new insights on diversification of this important vertebrate group.
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http://dx.doi.org/10.1371/currents.tol.2ca8041495ffafd0c92756e75247483eDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3682800PMC
April 2013

Addressing gene tree discordance and non-stationarity to resolve a multi-locus phylogeny of the flatfishes (Teleostei: Pleuronectiformes).

Syst Biol 2013 Sep 8;62(5):763-85. Epub 2013 Jun 8.

Department of Biological Sciences, The George Washington University, 2023 G St. NW, Washington, D.C. 20052, USA; College of Fisheries and Life Science, Shanghai Ocean University, Shanghai 201306, China; and National Systematics Laboratory NMFS/NOAA, Post Office Box 37012, Smithsonian Institution NHB, WC 60, MRC-153, Washington, D.C. 20013-7012, USA.

Non-homogeneous processes and, in particular, base compositional non-stationarity have long been recognized as a critical source of systematic error. But only a small fraction of current molecular systematic studies methodically examine and effectively account for the potentially confounding effect of non-stationarity. The problem is especially overlooked in multi-locus or phylogenomic scale analyses, in part because no efficient tools exist to accommodate base composition heterogeneity in large data sets. We present a detailed analysis of a data set with 20 genes and 214 taxa to study the phylogeny of flatfishes (Pleuronectiformes) and their position among percomorphs. Most genes vary significantly in base composition among taxa and fail to resolve flatfish monophyly and other emblematic groups, suggesting that non-stationarity may be causing systematic error. We show a strong association between base compositional bias and topological discordance among individual gene partitions and their inferred trees. Phylogenetic methods applying non-homogeneous models to accommodate non-stationarity have relatively minor effect to reduce gene tree discordance, suggesting that available computer programs applying these methods do not scale up efficiently to the data set of modest size analysed in this study. By comparing phylogenetic trees obtained with species tree (STAR) and concatenation approaches, we show that gene tree discordance in our data set is most likely due to base compositional biases than to incomplete lineage sorting. Multi-locus analyses suggest that the combined phylogenetic signal from all loci in a concatenated data set overcomes systematic biases induced by non-stationarity at each partition. Finally, relationships among flatfishes and their relatives are discussed in the light of these results. We find support for the monophyly of flatfishes and confirm findings from previous molecular phylogenetic studies suggesting their close affinity with several carangimorph groups (i.e., jack and allies, barracuda, archerfish, billfish and swordfish, threadfin, moonfish, beach salmon, and snook and barramundi).
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http://dx.doi.org/10.1093/sysbio/syt039DOI Listing
September 2013

The tree of life and a new classification of bony fishes.

PLoS Curr 2013 Apr 18;5. Epub 2013 Apr 18.

The George Washington University.

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.
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http://dx.doi.org/10.1371/currents.tol.53ba26640df0ccaee75bb165c8c26288DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3644299PMC
April 2013

Apparent signal of competition limiting diversification after ecological transitions from marine to freshwater habitats.

Ecol Lett 2012 Aug 6;15(8):822-30. Epub 2012 Jun 6.

Department of Biological Sciences, The George Washington University, Washington, DC 20052, USA.

Adaptive radiations are typically triggered when a lineage encounters a significant range of open niche space (ecological opportunity), stemming from colonisation of new areas, extinction of competitors or key innovations. The most well-known of these is the colonisation of new areas, through either dispersal into new regions or the invasion of novel ecological regimes. One aspect of ecological opportunity that has rarely been studied, however, is the extent to which pre-existent competitors act to limit diversification in newly colonised adaptive zones. Herein, we show that in multiple geographically independent invasions of freshwaters by marine Sea Catfishes (Ariidae), rates of both morphological disparification and lineage diversification are inversely related to the presence and diversity of other freshwater fish lineages. Only in one region (Australia-New Guinea) with an otherwise depauperate freshwater fauna, has an ariid invasion gained any substantial traction. This is true at both regional and community scales, suggesting that competitive constraints may be an important factor regulating adaptive radiation.
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http://dx.doi.org/10.1111/j.1461-0248.2012.01802.xDOI Listing
August 2012