Publications

2019
Cloutier A, Sackton TB, Grayson P, Clamp M, Baker AJ, Edwards SV. Whole-genome analyses resolve the phylogeny of flightless birds (Palaeognathae) in the presence of an empirical anomaly zone. Systematic Biology. 2019;10.1101/26.
Hu Z, Sackton TB, Edwards SV, Liu JS. Bayesian Detection of Convergent Rate Changes of Conserved Noncoding Elements on Phylogenetic Trees Pond SK. Molecular Biology and Evolution [Internet]. 2019. Publisher's Version
Sackton TB, Grayson P, Cloutier A, Hu Z, Liu JS, Wheeler NE, Gardner PP, Clarke JA, Baker AJ, Clamp M, et al. Convergent regulatory evolution and loss of flight in paleognathous birds. Science (New York, N.Y.) [Internet]. 2019;364 (6435) :74–78. Publisher's VersionAbstract
A core question in evolutionary biology is whether convergent phenotypic evolution is driven by convergent molecular changes in proteins or regulatory regions. We combined phylogenomic, developmental, and epigenomic analysis of 11 new genomes of paleognathous birds, including an extinct moa, to show that convergent evolution of regulatory regions, more so than protein-coding genes, is prevalent among developmental pathways associated with independent losses of flight. A Bayesian analysis of 284,001 conserved noncoding elements, 60,665 of which are corroborated as enhancers by open chromatin states during development, identified 2355 independent accelerations along lineages of flightless paleognaths, with functional consequences for driving gene expression in the developing forelimb. Our results suggest that the genomic landscape associated with morphological convergence in ratites has a substantial shared regulatory component.
Bravo GA, Antonelli A, Bacon CD, Bartoszek K, Blom MPK, Huynh S, Jones G, Knowles LL, Lamichhaney S, Marcussen T, et al. Embracing heterogeneity: coalescing the Tree of Life and the future of phylogenomics. PeerJ [Internet]. 2019;7 :e6399. Publisher's VersionAbstract
Building the Tree of Life (ToL) is a major challenge of modern biology, requiring advances in cyberinfrastructure, data collection, theory, and more. Here, we argue that phylogenomics stands to benefit by embracing the many heterogeneous genomic signals emerging from the first decade of large-scale phylogenetic analysis spawned by high-throughput sequencing (HTS). Such signals include those most commonly encountered in phylogenomic datasets, such as incomplete lineage sorting, but also those reticulate processes emerging with greater frequency, such as recombination and introgression. Here we focus specifically on how phylogenetic methods can accommodate the heterogeneity incurred by such population genetic processes; we do not discuss phylogenetic methods that ignore such processes, such as concatenation or supermatrix approaches or supertrees. We suggest that methods of data acquisition and the types of markers used in phylogenomics will remain restricted until a posteriori methods of marker choice are
2018
Liu L, Zhang J, Rheindt FR, Lei F, Qu Y, Wang Y, Zhang Y, Sullivan C, Nie W, Wang J, et al. Reply to Gatesy and Springer: Claims of homology errors and zombie lineages do not compromise the dating of placental diversification. Proceedings of the National Academy of Sciences. 2018;114 :E9433–E9434.
Antonelli A, Ariza M, Albert J, Andermann T, Azevedo J, Bacon C, Faurby S, Guedes T, Hoorn C, Lohmann LG, et al. Conceptual and empirical advances in Neotropical biodiversity research. PeerJ [Internet]. 2018;6 :e5644. Publisher's VersionAbstract
\textlessp\textgreaterThe unparalleled biodiversity found in the American tropics (the Neotropics) has attracted the attention of naturalists for centuries. Despite major advances in recent years in our understanding of the origin and diversification of many Neotropical taxa and biotic regions, many questions remain to be answered. Additional biological and geological data are still needed, as well as methodological advances that are capable of bridging these research fields. In this review, aimed primarily at advanced students and early-career scientists, we introduce the concept of “trans-disciplinary biogeography,” which refers to the integration of data from multiple areas of research in biology (e.g., community ecology, phylogeography, systematics, historical biogeography) and Earth and the physical sciences (e.g., geology, climatology, palaeontology), as a means to reconstruct the giant puzzle of Neotropical biodiversity and evolution in space and time. We caution against extrapolating results derived from the study of one or a few taxa to convey general scenarios of Neotropical evolution and landscape formation. We urge more coordination and integration of data and ideas among disciplines, transcending their traditional boundaries, as a basis for advancing tomorrow's ground-breaking research. Our review highlights the great opportunities for studying the Neotropical biota to understand the evolution of life.\textless/p\textgreater
Lewin HA, Robinson GE, Kress WJ, Baker WJ, Coddington J, Crandall KA, Durbin R, Edwards SV, Forest F, Gilbert MTP, et al. Earth BioGenome Project: Sequencing life for the future of life. Proceedings of the National Academy of Sciences [Internet]. 2018;115 (17) :4325–4333. Publisher's VersionAbstract
Increasing our understanding of Earth's biodiversity and responsibly stewarding its resources are among the most crucial scientific and social challenges of the new millennium. These challenges require fundamental new knowledge of the organization, evolution, functions, and interactions among millions of the planet's organisms. Herein, we present a perspective on the Earth BioGenome Project (EBP), a moonshot for biology that aims to sequence, catalog, and characterize the genomes of all of Earth's eukaryotic biodiversity over a period of 10 years. The outcomes of the EBP will inform a broad range of major issues facing humanity, such as the impact of climate change on biodiversity, the conservation of endangered species and ecosystems, and the preservation and enhancement of ecosystem services. We describe hurdles that the project faces, including data-sharing policies that ensure a permanent, freely available resource for future scientific discovery while respecting access and benefit sharing guidelines of the Nagoya Protocol. We also describe scientific and organizational challenges in executing such an ambitious project, and the structure proposed to achieve the project's goals. The far-reaching potential benefits of creating an open digital repository of genomic information for life on Earth can be realized only by a coordinated international effort.
Hoover B, Alcaide M, Jennings S, Sin SYW, Edwards SV, Nevitt GA. Ecology can inform genetics: Disassortative mating contributes to MHC polymorphism in Leach's storm-petrels (Oceanodroma leucorhoa). Molecular Ecology [Internet]. 2018;27 (16) :3371–3385. Publisher's VersionAbstract
Studies of MHC-based mate choice in wild populations often test hypotheses on species exhibiting female choice and male-male competition, which reflects the general prevalence of females as the choosy sex in natural systems. Here, we examined mutual mate-choice patterns in a small burrow-nesting seabird, the Leach's storm-petrel (Oceanodroma leucorhoa), using the major histocompatibility complex (MHC). The life history and ecology of this species are extreme: both partners work together to fledge a single chick during the breeding season, a task that requires regularly travelling hundreds of kilometres to and from foraging grounds over a 6- to 8-week provisioning period. Using a 5-year data set unprecedented for this species (n = 1078 adults and 925 chicks), we found a positive relationship between variation in the likelihood of female reproductive success and heterozygosity at Ocle-DAB2, a MHC class IIB locus. Contrary to previous reports rejecting disassortative mating as a mechanism for maintaining genetic polymorphism in this species, here we show that males make significant disassortative mate-choice decisions. Variability in female reproductive success suggests that the most common homozygous females (Ocle-DAB2*01/Ocle-DAB2*01) may be physiologically disadvantaged and, therefore, less preferred as lifelong partners for choosy males. The results from this study support the role of mate choice in maintaining high levels of MHC variability in a wild seabird species and highlight the need to incorporate a broader ecological framework and sufficient sample sizes into studies of MHC-based mating patterns in wild populations in general.
Schmitt CJ, Cook JA, Zamudio KR, Edwards SV. Museum specimens of terrestrial vertebrates are sensitive indicators of environmental change in the Anthropocene. Philosophical Transactions of the Royal Society B: Biological Sciences [Internet]. 2018;374 (1763) :20170387. Publisher's VersionAbstract
Natural history museums and the specimen collections they curate are vital scientific infrastructure, a fact as true today as it was when biologists began collecting and preserving specimens over 200 years ago. The importance of museum specimens in studies of taxonomy, systematics, ecology and evolutionary biology is evidenced by a rich and abundant literature, yet creative and novel uses of specimens are constantly broadening the impact of natural history collections on biodiversity science and global sustainability. Excellent examples of the critical importance of specimens come from their use in documenting the consequences of environmental change, which is particularly relevant considering the alarming rate at which we now modify our planet in the Anthropocene. In this review, we highlight the important role of bird, mammal and amphibian specimens in documenting the Anthropocene and provide examples that underscore the need for continued collection of museum specimens.This article is part of the theme issue 'Biological collections for understanding biodiversity in the Anthropocene'.
Tang Q, Edwards SV, Rheindt FE. Rapid diversification and hybridization have shaped the dynamic history of the genus Elaenia. Molecular phylogenetics and evolution [Internet]. 2018;127 :522–533. Publisher's VersionAbstract
Multi-locus data have proven invaluable in phylogenetic reconstruction and species delimitation. However, the mixed genetic signal from different loci can make inference of evolutionary history challenging and may produce incongruences depending on analytical and marker choice. Aside from incomplete lineage sorting (ILS) following diversification events that have had little time for deep differentiation, the most common causes of incongruent phylogenies are genetic introgression confounding a bifurcating evolutionary trajectory. In this study, we used multi-locus analytical approaches on sequence data of nine loci from 80 individuals of over 20 Neotropical Elaenia flycatcher species to examine the systematics, molecular phylogeny and species limits of this complex genus. Our results provide a robust phylogeny and estimates of species limits within Elaenia, but point to important cases of incongruences among phylogenies based on different analytical approaches. Simulations and estimates of divergence times provide reasonable explanations for the incongruent placement of some Elaenia taxa, pointing to multiple cases of both ILS and introgression within the genus. Molecular dating of major evolutionary events revealed intensive diversification during the Pleistocene, suggesting a central role of climate oscillations in the evolution of Elaenia flycatchers.
Ezaz T, Edwards SV. Editorial: Evolutionary Feedbacks Between Population Biology and Genome Architecture. Frontiers in Genetics [Internet]. 2018;9 :329. Publisher's Version
Wu S, Edwards S, Liu L. Genome-scale DNA sequence data and the evolutionary history of placental mammals. Data in Brief [Internet]. 2018;18 :1972–1975. Publisher's VersionAbstract
We present a genomic data set comprised of the coding DNA sequences of 5162 loci from 90 vertebrate species, including 82 mammals. The loci were aligned with their protein sequences. The aligned protein sequences were then back translated into their original DNA sequences. The alignments were further filtered to remove individual sequences from each alignment exhibiting long branches or other unusual features. The data is deposited in figshare (http://figshare.com/articles/cds\_5162.zip/6031190) and will be useful as a test data set for large-scale phylogenomic analysis.
Perry BW, Card DC, McGlothlin JW, Pasquesi GIM, Adams RH, Schield DR, Hales NR, Corbin AB, Demuth JP, Hoffmann FG, et al. Molecular Adaptations for Sensing and Securing Prey and Insight into Amniote Genome Diversity from the Garter Snake Genome O'Connell M. Genome Biology and Evolution [Internet]. 2018;10 (8) :2110–2129. Publisher's VersionAbstract
Colubridae represents the most phenotypically diverse and speciose family of snakes, yet no well-assembled and annotated genome exists for this lineage. Here, we report and analyze the genome of the garter snake, Thamnophis sirtalis, a colubrid snake that is an important model species for research in evolutionary biology, physiology, genomics, behavior, and the evolution of toxin resistance. Using the garter snake genome, we show how snakes have evolved numerous adaptations for sensing and securing prey, and identify features of snake genome structure that provide insight into the evolution of amniote genomes. Analyses of the garter snake and other squamate reptile genomes highlight shifts in repeat element abundance and expansion within snakes, uncover evidence of genes under positive selection, and provide revised neutral substitution rate estimates for squamates. Our identification of Z and W sex chromosome-specific scaffolds provides evidence for multiple origins of sex chromosome systems in snakes and demonstrates the value of this genome for studying sex chromosome evolution. Analysis of gene duplication and loss in visual and olfactory gene families supports a dim-light ancestral condition in snakes and indicates that olfactory receptor repertoires underwent an expansion early in snake evolution. Additionally, we provide some of the first links between secreted venom proteins, the genes that encode them, and their evolutionary origins in a rear-fanged colubrid snake, together with new genomic insight into the coevolutionary arms race between garter snakes and highly toxic newt prey that led to toxin resistance in garter snakes.
Campbell-Staton SC, Bare A, Losos JB, Edwards SV, Cheviron ZA. Physiological and regulatory underpinnings of geographic variation in reptilian cold tolerance across a latitudinal cline. Molecular Ecology [Internet]. 2018;27 (9) :2243–2255. Publisher's VersionAbstract
Understanding the mechanisms that produce variation in thermal performance is a key component to investigating climatic effects on evolution and adaptation. However, disentangling the effects of local adaptation and phenotypic plasticity in shaping patterns of geographic variation in natural populations can prove challenging. Additionally, the physiological mechanisms that cause organismal dysfunction at extreme temperatures are still largely under debate. Using the green anole, Anolis carolinensis, we integrate measures of cold tolerance (CTmin ), standard metabolic rate, heart size, blood lactate concentration and RNAseq data from liver tissue to investigate geographic variation in cold tolerance and its underlying mechanisms along a latitudinal cline. We found significant effects of thermal acclimation and latitude of origin on variation in cold tolerance. Increased cold tolerance correlates with decreased rates of oxygen consumption and blood lactate concentration (a proxy for oxygen limitation), suggesting elevated performance is associated with improved oxygen economy during cold exposure. Consistent with these results, co-expression modules associated with blood lactate concentration are enriched for functions associated with blood circulation, coagulation and clotting. Expression of these modules correlates with thermal acclimation and latitude of origin. Our findings support the oxygen and capacity-limited thermal tolerance hypothesis as a potential contributor to variation in reptilian cold tolerance. Moreover, differences in gene expression suggest regulation of the blood coagulation cascade may play an important role in reptilian cold tolerance and may be the target of natural selection in populations inhabiting colder environments.
2017
Ghanem M, Wang L, Zhang Y, Edwards S, Lu A, Ley D, El-Gazzar M. Core Genome Multilocus Sequence Typing: a Standardized Approach for Molecular Typing of Mycoplasma gallisepticum Fenwick B. Journal of Clinical Microbiology [Internet]. 2017;56 (1). Publisher's VersionAbstract
\textlessp\textgreater \textlessnamed-content content-type="genus-species"\textgreaterMycoplasma gallisepticum\textless/named-content\textgreater is the most virulent and economically important \textlessnamed-content content-type="genus-species"\textgreaterMycoplasma\textless/named-content\textgreater species for poultry worldwide. Currently, \textlessnamed-content content-type="genus-species"\textgreaterM. gallisepticum\textless/named-content\textgreater strain differentiation based on sequence analysis of 5 loci remains insufficient for accurate outbreak investigation. Recently, whole-genome sequences (WGS) of many human and animal pathogens have been successfully used for microbial outbreak investigations. However, the massive sequence data and the diverse properties of different genes within bacterial genomes results in a lack of standard reproducible methods for comparisons among \textlessnamed-content content-type="genus-species"\textgreaterM. gallisepticum\textless/named-content\textgreater whole genomes. Here, we proposed the development of a core genome multilocus sequence typing (cgMLST) scheme for \textlessnamed-content content-type="genus-species"\textgreaterM. gallisepticum\textless/named-content\textgreater strains and field isolates. For development of this scheme, a diverse collection of 37 \textlessnamed-content content-type="genus-species"\textgreaterM. gallisepticum\textless/named-content\textgreater genomes was used to identify cgMLST targets. A total of 425 \textlessnamed-content content-type="genus-species"\textgreaterM. gallisepticum\textless/named-content\textgreater conserved genes (49.85% of \textlessnamed-content content-type="genus-species"\textgreaterM. gallisepticum\textless/named-content\textgreater genome) were selected as core genome targets. A total of 81 \textlessnamed-content content-type="genus-species"\textgreaterM. gallisepticum\textless/named-content\textgreater genomes from 5 countries on 4 continents were typed using \textlessnamed-content content-type="genus-species"\textgreaterM. gallisepticum\textless/named-content\textgreater cgMLST. Analyses of phylogenetic trees generated by cgMLST displayed a high degree of agreement with geographical and temporal information. Moreover, the high discriminatory power of cgMLST allowed differentiation between \textlessnamed-content content-type="genus-species"\textgreaterM. gallisepticum\textless/named-content\textgreater strains of the same outbreak. \textlessnamed-content content-type="genus-species"\textgreaterM. gallisepticum\textless/named-content\textgreater cgMLST represents a standardized, accurate, highly discriminatory, and reproducible method for differentiation among \textlessnamed-content content-type="genus-species"\textgreaterM. gallisepticum\textless/named-content\textgreater isolates. cgMLST provides stable and expandable nomenclature, allowing for comparison and sharing of typing results among laboratories worldwide. cgMLST offers an opportunity to harness the tremendous power of next-generation sequencing technology in applied avian mycoplasma epidemiology at both local and global levels. \textless/p\textgreater
Chattopadhyay B, Garg KM, Gwee CY, Edwards SV, Rheindt FE. Gene flow during glacial habitat shifts facilitates character displacement in a Neotropical flycatcher radiation. BMC Evolutionary Biology [Internet]. 2017;17 (1) :210. Publisher's VersionAbstract
Pleistocene climatic fluctuations are known to be an engine of biotic diversification at higher latitudes, but their impact on highly diverse tropical areas such as the Andes remains less well-documented. Specifically, while periods of global cooling may have led to fragmentation and differentiation at colder latitudes, they may – at the same time – have led to connectivity among insular patches of montane tropical habitat with unknown consequences on diversification. In the present study we utilized \~5.5 kb of DNA sequence data from eight nuclear loci and one mitochondrial gene alongside diagnostic morphological and bioacoustic markers to test the effects of Pleistocene climatic fluctuations on diversification in a complex of Andean tyrant-flycatchers of the genus Elaenia. Population genetic and phylogenetic approaches coupled with coalescent simulations demonstrated disparate levels of gene flow between the taxon chilensis and two parapatric Elaenia taxa predominantly during the last glacial period but not thereafter, possibly on account of downward shifts of montane forest habitat linking the populations of adjacent ridges. Additionally, morphological and bioacoustic analyses revealed a distinct pattern of character displacement in coloration and vocal traits between the two sympatric taxa albiceps and pallatangae, which were characterized by a lack of gene flow. Our study demonstrates that global periods of cooling are likely to have facilitated gene flow among Andean montane Elaenia flycatchers that are more isolated from one another during warm interglacial periods such as the present era. We also identify a hitherto overlooked case of plumage and vocal character displacement, underpinning the complexities of gene flow patterns caused by Pleistocene climate change across the Andes.
Liu L, Zhang J, Rheindt FE, Lei F, Qu Y, Wang Y, Zhang Y, Sullivan C, Nie W, Wang J, et al. Genomic evidence reveals a radiation of placental mammals uninterrupted by the KPg boundary. PNAS [Internet]. 2017;114 (35) :E7282-E7290. Open Access Download
Termignoni-Garcia F, Jaramillo-Correa JP, Chable-Santos J, Liu M, Shultz AJ, Edwards SV, Escalante-Pliego P. Genomic footprints of adaptation in a cooperatively breeding tropical bird across a vegetation gradient. Molecular Ecology. 2017;26 (17) :4483-4496. PDF
Tigano A, Shultz AJ, Edwards SV, Robertson GJ, Friesen VL. Outlier analyses to test for local adaptation to breeding grounds in a migratory arctic seabird. Ecology and Evolution [Internet]. 2017;7 (7) :2370-2381. Open Access Download
Edwards SV, Cloutier AC, Baker AJ. Conserved Nonexonic Elements : A Novel Class of Marker for Phylogenomics. Systematic Biology [Internet]. 2017;66 (October) :1028–1044. Open Access DownloadAbstract
Noncoding markers have a particular appeal as tools for phylogenomic analysis because, at least in vertebrates, they appear less subject to strong variation in GC content among lineages. Thus far, ultraconserved elements (UCEs) and introns have been the most widely used noncoding markers. Here we analyze and study the evolutionary properties of a new type of noncoding marker, conserved nonexonic elements (CNEEs), which consists of noncoding elements that are estimated to evolve slower than the neutral rate across a set of species. Although they often include UCEs, CNEEs are distinct from UCEs because they are not ultraconserved, and, most importantly, the core region alone is analyzed, rather
than both the core and its flanking regions. Using a data set of 16 birds plus an alligator outgroup, and ∼3600–∼3800 loci per marker type, we found that although CNEEs were less variable than bioinformatically derived UCEs or introns and in some cases exhibited a slower approach to branch resolution as determined by phylogenomic subsampling, the quality of CNEE alignmentswas superior to those of the other markers, with fewer gaps and missing species. Phylogenetic resolution using coalescent approaches was comparable among the three marker types, with most nodes being fully and congruently resolved. Comparison of phylogenetic results across the three marker types indicated that one branch, the sister group to the
passerine+falcon clade,was resolved differently and with moderate (>70%) bootstrap support between CNEEs and UCEs or introns. Overall, CNEEs appear to be promising as phylogenomic markers, yielding phylogenetic resolution as high as for UCEs and introns but with fewer gaps, less ambiguity in alignments and with patterns of nucleotide substitution more consistent with the assumptions of commonly used methods of phylogenetic analysis.

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