Publications by authors named "Lily C Hughes"

9 Publications

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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

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

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

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

Transcriptomic differentiation underlying marine-to-freshwater transitions in the South American silversides and (Atheriniformes).

Ecol Evol 2017 07 7;7(14):5258-5268. Epub 2017 Jun 7.

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

Salinity gradients are critical habitat determinants for freshwater organisms. Silverside fishes in the genus have recently and repeatedly transitioned from marine to freshwater habitats, overcoming a strong ecological barrier. Genomic and transcriptomic changes involved in this kind of transition are only known for a few model species. We present new data and analyses of gene expression and microbiome composition in the gills of two closely related silverside species, marine and freshwater and find more than three thousand transcripts differentially expressed, with osmoregulatory/ion transport genes and immune genes showing very different expression patterns across species. Interspecific differences also involve more than one thousand transcripts with nonsynonymous SNPs in the coding sequences, most of which were not differentially expressed. In addition to characterizing gill transcriptomes from wild-caught marine and freshwater fishes, we test experimentally the response to salinity increases by collected from freshwater habitats. Patterns of expression in gill transcriptomes of exposed to high salinity do not resemble mRNA expression, suggesting lack of plasticity for adaptation to marine conditions in this species. The diversity of functions associated with both the differentially expressed set of transcripts and those with sequence divergence plus marked microbiome differences suggest that multiple abiotic and biotic factors in marine and freshwater habitats are driving transcriptomic differences between these species.
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http://dx.doi.org/10.1002/ece3.3133DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5528240PMC
July 2017

Kisspeptin system in pejerrey fish (Odontesthes bonariensis). Characterization and gene expression pattern during early developmental stages.

Comp Biochem Physiol A Mol Integr Physiol 2017 02 23;204:146-156. Epub 2016 Nov 23.

Instituto de Investigaciones Biotecnológicas-Instituto Tecnológico de Chascomús (IIB-INTECH), CONICET-UNSAM, Chascomús, Argentina. Electronic address:

In vertebrates, kisspeptins and their receptors are known to be related to puberty onset and gonadal maturation, however, there are few studies concerning their role in early development. Here, we characterize the kisspeptin system in the pejerrey, Odontesthes bonariensis, a fish with strong temperature-dependent sex determination. We reconstructed the phylogenetic history of the two ligands (kiss1 and kiss 2) and two receptors (kissr2 and kissr3) in pejerrey in the context of recent classifications of bony fishes, determined their tissue distribution and documented the early expression pattern of these ligands and receptors. Phylogenetic analysis of these gene families clearly resolved the percomorph clade and grouped pejerrey with Beloniformes. Paralogous sets of genes putatively arising from the teleost-specific genome duplication event (3R) were not detected. Kisspeptins and their receptors showed a wide tissue distribution in adult pejerrey, including tissues not related to reproduction. In larvae reared at 24°C, the four kisspeptin elements were expressed in the head from week 1 to week 8 of life, with no differences in transcript levels. Larvae kept at a female-producing temperature (17°C) did not show statistically significant differences in the transcript levels of all analyzed genes during the sex determination/differentiation period; however, in those larvae raised at male producing temperature (29°C), kiss2 levels were increased at week 4 after hatching. These results showed that all members of the kisspeptin system are expressed at this early period, and the increase of kiss2 transcripts at week 4 could be interpreted as it would be related to the differentiation of the brain-pituitary axis in male development.
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http://dx.doi.org/10.1016/j.cbpa.2016.11.014DOI Listing
February 2017

Multi-locus fossil-calibrated phylogeny of Atheriniformes (Teleostei, Ovalentaria).

Mol Phylogenet Evol 2015 May 10;86:8-23. Epub 2015 Mar 10.

Department of Biological Sciences, The George Washington University, Washington, DC, USA. Electronic address:

Phylogenetic relationships among families within the order Atheriniformes have been difficult to resolve on the basis of morphological evidence. Molecular studies so far have been fragmentary and based on a small number taxa and loci. In this study, we provide a new phylogenetic hypothesis based on sequence data collected for eight molecular markers for a representative sample of 103 atheriniform species, covering 2/3 of the genera in this order. The phylogeny is calibrated with six carefully chosen fossil taxa to provide an explicit timeframe for the diversification of this group. Our results support the subdivision of Atheriniformes into two suborders (Atherinopsoidei and Atherinoidei), the nesting of Notocheirinae within Atherinopsidae, and the monophyly of tribe Menidiini, among others. We propose taxonomic changes for Atherinopsoidei, but a few weakly supported nodes in our phylogeny suggests that further study is necessary to support a revised taxonomy of Atherinoidei. The time-calibrated phylogeny was used to infer ancestral habitat reconstructions to explain the current distribution of marine and freshwater taxa. Based on these results, the current distribution of Atheriniformes is likely due to widespread marine dispersal along the margins of continents, infrequent trans-oceanic dispersal, and repeated invasion of freshwater habitats. This conclusion is supported by post-Gondwanan divergence times among families within the order, and a high probability of a marine ancestral habitat.
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http://dx.doi.org/10.1016/j.ympev.2015.03.001DOI Listing
May 2015