Publications

2013
Janes DE, Elsey RM, Langan EM, Valenzuela N, Edwards SV. Sex-Biased Expression of Sex-Differentiating Genes FOXL2 and FGF9 in American Alligators, Alligator mississippiensis. Sexual Development [Internet]. 2013;7 (5) :253-260. Publisher's Version PDF
2012
Campbell-Staton SC, Goodman RM, Backstroem N, Edwards SV, Losos JB, Kolbe JJ. Out of Florida: mtDNA reveals patterns of migration and Pleistocene range expansion of the Green Anole lizard (Anolis carolinensis). Ecology and Evolution. 2012;2 (9) :2274-2284.Abstract
Anolis carolinensis is an emerging model species and the sole member of its genus native to the United States. Considerable morphological and physiological variation has been described in the species, and the recent sequencing of its genome makes it an attractive system for studies of genome variation. To inform future studies of molecular and phenotypic variation within A. carolinensis, a rigorous account of intraspecific population structure and relatedness is needed. Here, we present the most extensive phylogeographic study of this species to date. Phylogenetic analyses of mitochondrial DNA sequence data support the previous hypothesis of a western Cuban origin of the species. We found five well-supported, geographically distinct mitochondrial haplotype clades throughout the southeastern United States. Most Florida populations fall into one of three divergent clades, whereas the vast majority of populations outside Florida belong to a single, shallowly diverged clade. Genetic boundaries do not correspond to major rivers, but may reflect effects of Pleistocene glaciation events and the Appalachian Mountains on migration and expansion of the species. Phylogeographic signal should be examined using nuclear loci to complement these findings.
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Anderson C, Liu L, Pearl D, Edwards, S. V. Tangled Trees: The challenge of inferring species trees from coalescent and non-coalescent genes. In: Anisimova M Evolutionary Genomics: Statistical and Computational Methods, volume 2. New York: Springer ; 2012. pp. 3-28.
Zhang Q, Edwards SV. The evolution of intron size in amniotes: a role for powered flight?. Genome Biology and Evolution. 2012.Abstract

Intronic DNA is a major component of eukaryotic genes and genomes and can be subject to selective constraint and have functions in gene regulation. Intron size is of particular interest given that it is thought to be the target of a variety of evolutionary forces and has been suggested to be linked ultimately to various phenotypic traits, such as powered flight. Using whole-genome analyses and comparative approaches that account for phylogenetic nonindependence, we examined interspecific variation in intron size variation in three data sets encompassing from 12 to 30 amniotes genomes and allowing for different levels of genome coverage. In addition to confirming that intron size is negatively associated with intron position and correlates with genome size, we found that on average mammals have longer introns than birds and nonavian reptiles, a trend that is correlated with the proliferation of repetitive elements in mammals. Two independent comparisons between flying and nonflying sister groups both showed a reduction of intron size in volant species, supporting an association between powered flight, or possibly the high metabolic rates associated with flight, and reduced intron/genome size. Small intron size in volant lineages is less easily explained as a neutral consequence of large effective population size. In conclusion, we found that the evolution of intron size in amniotes appears to be non-neutral, is correlated with genome size, and is likely influenced by powered flight and associated high metabolic rates.

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Bonneaud C, Balenger SL, Zhang J, Edwards SV, Hill GE. Innate immunity and the evolution of resistance to an emerging infectious disease in a wild bird. Molecular Ecology. 2012;21 :2628-2639.Abstract

Innate immunity is expected to play a primary role in conferring resistance to novel infectious diseases, but few studies have attempted to examine its role in the evolution of resistance to emerging pathogens in wild vertebrate populations. Here, we used experimental infections and cDNA microarrays to examine whether changes in the innate and/or acquired immune responses likely accompanied the emergence of resistance in house finches (Carpodacus mexicanus) in the eastern United States subject to a recent outbreak of conjunctivitis-causing bacterium (Mycoplasma gallisepticum—MG). Three days following experimental infection with MG, we observed differences in the splenic transcriptional responses between house finches from eastern U.S. populations, with a 12-year history of MG exposure, versus western U.S. populations, with no history of exposure to MG. In particular, western birds down-regulated gene expression, while eastern finches showed no expression change relative to controls. Studies involving poultry have shown that MG can manipulate host immunity, and our observations suggest that pathogen manipulation occurred only in finches from the western populations, outside the range of MG. Fourteen days after infection, eastern finches, but not western finches, up-regulated genes associated with acquired immunity (cell-mediated immunity) relative to controls. These observations suggest population differences in the temporal course of the response to infection with MG and imply that innate immune processes were targets of selection in response to MG in the eastern U.S. population.

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Wu S, Wu W, Zhang F, Ye J, Ni X, Sun J, Edwards SV, Meng J, Organ CL. Molecular and Paleontological Evidence for a Post-Cretaceous Origin of Rodents. Plos One. 2012;7 :e46445.Abstract
The timing of the origin and diversification of rodents remains controversial, due to conflicting results from molecular clocks
and paleontological data. The fossil record tends to support an early Cenozoic origin of crown-group rodents. In contrast,
most molecular studies place the origin and initial diversification of crown-Rodentia deep in the Cretaceous, although some
molecular analyses have recovered estimated divergence times that are more compatible with the fossil record. Here we attempt to resolve this conflict by carrying out a molecular clock investigation based on a nine-gene sequence dataset and a novel set of seven fossil constraints, including two new rodent records (the earliest known representatives of Cardiocraniinae and Dipodinae). Our results indicate that rodents originated around 61.7–62.4 Ma, shortly after the Cretaceous/Paleogene (K/Pg) boundary, and diversified at the intraordinal level around 57.7–58.9 Ma. These estimates are broadly consistent with the paleontological record, but challenge previous molecular studies that place the origin and early diversification of rodents in the Cretaceous. This study demonstrates that, with reliable fossil constraints, the  incompatibility between paleontological and molecular estimates of rodent divergence times can be eliminated using currently available tools and genetic markers. Similar conflicts between molecular and paleontological evidence bedevil attempts to establish the origination times of other placental groups. The example of the present study suggests that more reliable fossil calibration points may represent the key to resolving these controversies.
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Song S, Liu L, Edwards SV, Wu SY. Resolving conflict in eutherian mammal phylogeny using phylogenomics and the multispecies coalescent model. Proceedings of the National Academy of Sciences of the United States of America. 2012;109 :14942-14947.Abstract

The reconstruction of the Tree of Life has relied almost entirely on concatenation methods, which do not accommodate gene tree heterogeneity, a property that simulations and theory have identified as a likely cause of incongruent phylogenies. However, this incongruence has not yet been demonstrated in empirical studies. Several key relationships among eutherian mammals remain controversial and conflicting among previous studies, including the root of eutherian tree and the relationships within Euarchontoglires and Laurasiatheria. Both Bayesian and maximum-likelihood analysis of genome-wide data of 447 nuclear genes from 37 species show that concatenation methods indeed yield strong incongruence in the phylogeny of eutherian mammals, as revealed by subsampling analyses of loci and taxa, which produced strongly conflicting topologies. In contrast, the coalescent methods, which accommodate gene tree heterogeneity, yield a phylogeny that is robust to variable gene and taxon sampling and is congruent with geographic data. The data also demonstrate that incomplete lineage sorting, a major source of gene tree heterogeneity, is relevant to deep-level phylogenies, such as those among eutherian mammals. Our results firmly place the eutherian root between Atlantogenata and Boreoeutheria and support ungulate polyphyly and a sister-group relationship between Scandentia and Primates. This study demonstrates that the incongruence introduced by concatenation methods is a major cause of long-standing uncertainty in the phylogeny of eutherian mammals, and the same may apply to other clades. Our analyses suggest that such incongruence can be resolved using phylogenomic data and coalescent methods that deal explicitly with gene tree heterogeneity.

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St John J, Braun E, Isberg S, Miles L, Chong A, Gongora J, Dalzell P, Moran C, Bed'Hom B, Abzhanov A, et al. Sequencing three crocodilian genomes to illuminate the evolution of archosaurs and amniotes. Genome Biology. 2012;13 :415.Abstract

The International Crocodilian Genomes Working Group (ICGWG) will sequence and assemble the American alligator (Alligator mississippiensis), saltwater crocodile (Crocodylus porosus) and Indian gharial (Gavialis gangeticus) genomes. The status of these projects and our planned analyses are described.

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Lee JY, Joseph L, Edwards SV. A Species Tree for the Australo-Papuan Fairy-wrens and Allies (Aves: Maluridae). Systematic Biology. 2012;61 :253-271.Abstract

We explored the efficacy of species tree methods at the family level in birds, using the Australo-Papuan Fairy-wrens (Passeriformes: Maluridae) as a model system. Fairy-wrens of the genus Malurus are known for high intensities of sexual selection, resulting in some cases in rapid speciation. This history suggests that incomplete lineage sorting (ILS) of neutrally evolving loci could be substantial, a situation that could compromise traditional methods of combining loci in phylogenetic analysis. Using 18 molecular markers (5 anonymous loci, 7 exons, 5 introns, and 1 mitochondrial DNA locus), we show that gene tree monophyly across species could be rejected for 16 of 18 loci, suggesting substantial ILS at the family level in these birds. Using the software Concaterpillar, we also detect three statistically distinct clusters of gene trees among the 18 loci. Despite substantial variation in gene trees, species trees constructed using four different species tree estimation methods (BEST, BUCKy, and STAR) were generally well supported and similar to each other and to the concatenation tree, with a few mild discordances at nodes that could be explained by rapid and recent speciation events. By contrast, minimizing deep coalescences produced a species tree that was topologically more divergent from those of the other methods as measured by multidimensional scaling of trees. Additionally, gene and species trees were topologically more similar in the BEST analysis, presumably because of the species tree prior employed in BEST which appropriately assumes that gene trees are correlated with each other and with the species tree. Among the 18 loci, we also discovered 102 independent indel markers, which also proved phylogenetically informative, primarily among genera, and displayed a ∼4-fold bias towards deletions. As suggested in earlier work, the grasswrens (Amytornis) are sister to the rest of the family and the emu-wrens (Stipiturus) are sister to fairy-wrens (Malurus, Clytomyias). Our study shows that ILS is common at the family level in birds yet, despite this, species tree methods converge on broadly similar results for this family.

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Küpper C, Augustin J, Edwards S, Székely T, Kosztolányi A, Burke T, Janes DE. Triploid plover female provides support for a role of the W chromosome in avian sex determination. Biology Letters. 2012;8 :787-789.Abstract

Two models, Z Dosage and Dominant W, have been proposed to explain sex determination in birds, in which males are characterized by the presence of two Z chromosomes, and females are hemizygous with a Z and a W chromosome. According to the Z Dosage model, high dosage of a Z-linked gene triggers male development, whereas the Dominant W model postulates that a still unknown W-linked gene triggers female development. Using 33 polymorphic microsatellite markers, we describe a female triploid Kentish plover Charadrius alexandrinus identified by characteristic triallelic genotypes at 14 autosomal markers that produced viable diploid offspring. Chromatogram analysis showed that the sex chromosome composition of this female was ZZW. Together with two previously described ZZW female birds, our results suggest a prominent role for a female determining gene on the W chromosome. These results imply that avian sex determination is more dynamic and complex than currently envisioned.

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Delaney NF, Balenger S, Bonneaud C, Marx CJ, Hill GE, Ferguson-Noel N, Tsai P, Rodrigo A, Edwards SV. Ultrafast Evolution and Loss of CRISPRs Following a Host Shift in a Novel Wildlife Pathogen, Mycoplasma gallisepticum. PLoS Genetics. 2012;8 :e1002511.Abstract

Author Summary

Documenting the evolutionary changes occurring in pathogens when they switch hosts is important for understanding mechanisms of adaptation and rates of evolution. We took advantage of a novel host–pathogen system involving a bacterial pathogen (Mycoplasma gallisepticum, or MG) and a songbird host, the House Finch, to study genome-wide changes during a host-shift. Around 1994, biologists noticed that House Finches were contracting conjunctivitis and MG from poultry was discovered to be the cause. The resulting epizootic was one of the best documented for a wildlife species, partly as a result of thousands of citizen science observers. We sequenced the genomes of 12 House Finch MG strains sampled throughout the epizootic, from 1994–2007, as well as four additional putatively ancestral poultry MG strains. Using this serial sample, we estimate a remarkably high rate of substitution, consistent with past implications that mycoplasmas are among the fastest evolving bacteria. We also find that an array of likely phage-derived sequences known as CRISPRs has degraded and ceased to recruit new repeats in the House Finch MG strains, as compared to the poultry strains in which it is diverse and rapidly evolving. This suggests that phage dynamics might be important in the dynamics of MG infection.

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Chen KH, Rusch M, Edwards SV, Rizzo M, Anderson SW. Ventromedial prefrontal cortex modulates social pressure effects on decision-making while driving. Society for Neuroscience Abstract Viewer and Itinerary Planner [Internet]. 2012;42. Publisher's Version
Bonneaud C, Balenger SL, Zhang J, Edwards SV, Hill GE. Innate immunity and the evolution of resistance to an emerging infectious disease in a wild bird. Molecular Ecology [Internet]. 2012;21 (11) :2628-2639. Publisher's VersionAbstract

Innate immunity is expected to play a primary role in conferring resistance to novel infectious diseases, but few studies have attempted to examine its role in the evolution of resistance to emerging pathogens in wild vertebrate populations. Here, we used experimental infections and cDNA microarrays to examine whether changes in the innate and/or acquired immune responses likely accompanied the emergence of resistance in house finches (Carpodacus mexicanus) in the eastern United States subject to a recent outbreak of conjunctivitis-causing bacterium (Mycoplasma gallisepticum—MG). Three days following experimental infection with MG, we observed differences in the splenic transcriptional responses between house finches from eastern U.S. populations, with a 12-year history of MG exposure, versus western U.S. populations, with no history of exposure to MG. In particular, western birds down-regulated gene expression, while eastern finches showed no expression change relative to controls. Studies involving poultry have shown that MG can manipulate host immunity, and our observations suggest that pathogen manipulation occurred only in finches from the western populations, outside the range of MG. Fourteen days after infection, eastern finches, but not western finches, up-regulated genes associated with acquired immunity (cell-mediated immunity) relative to controls. These observations suggest population differences in the temporal course of the response to infection with MG and imply that innate immune processes were targets of selection in response to MG in the eastern U.S. population.

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Delaney NF, Balenger S, Bonneaud C, Marx CJ, Hill GE, Ferguson-Noel N, Tsai P, Rodrigo A, Edwards SV. Ultrafast Evolution and Loss of CRISPRs Following a Host Shift in a Novel Wildlife Pathogen, Mycoplasma gallisepticum. Plos Genetics [Internet]. 2012;8 (2). Publisher's VersionAbstract
Measureable rates of genome evolution are well documented in human pathogens but are less well understood in bacterial
pathogens in the wild, particularly during and after host switches.
Mycoplasma gallisepticum
(MG) is a pathogenic bacterium
that has evolved predominantly in poultry and recently jumped to wild house finches (
Carpodacus mexicanus
), a common
North American songbird. For the first time we characterize the genome and measure rates of genome evolution in House
Finch isolates of MG, as well as in poultry outgroups. Using whole-genome sequences of 12 House Finch isolates across a
13-year serial sample and an additional four newly sequenced poultry strains, we estimate a nucleotide diversity in House
Finch isolates of only
,
2% of ancestral poultry strains and a nucleotide substitution rate of 0.8
2
1.2
6
10
2
5
per site per year
both in poultry and in House Finches, an exceptionally fast rate rivaling some of the highest estimates reported thus far for
bacteria. We also found high diversity and complete turnover of CRISPR arrays in poultry MG strains prior to the switch to
the House Finch host, but after the invasion of House Finches there is progressive loss of CRISPR repeat diversity, and
recruitment of novel CRISPR repeats ceases. Recent (2007) House Finch MG strains retain only
,
50% of the CRISPR
repertoire founding (1994–95) strains and have lost the CRISPR–associated genes required for CRISPR function. Our results
suggest that genome evolution in bacterial pathogens of wild birds can be extremely rapid and in this case is accompanied

by apparent functional loss of CRISPRs

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2011
Organ CL, Edwards SV. Major events in genome evolution. In: Dyke G, Kaiser G Living Dinosaurs: The Evolutionary History of Modern Birds. Hoboken, NJ: John Wiley & Sons, Ltd. ; 2011. pp. 325-337.
Rheindt FE, Székely T, Edwards SV, Lee PLM, Burke T, Kennerley PR, Bakewell DN, Alrashidi M, Kosztolányi A, Weston MA, et al. Conflict between Genetic and PhenotypicDifferentiation: The Evolutionary History of a ‘Lost and Rediscovered’ Shorebird. Plos One. 2011;6 :e26995.Abstract

Understanding and resolving conflicts between phenotypic and genetic differentiation is central to evolutionary research. While phenotypically monomorphic species may exhibit deep genetic divergences, some morphologically distinct taxa lack notable genetic differentiation. Here we conduct a molecular investigation of an enigmatic shorebird with a convoluted taxonomic history, the White-faced Plover (Charadrius alexandrinus dealbatus), widely regarded as a subspecies of the Kentish Plover (C. alexandrinus). Described as distinct in 1863, its name was consistently misapplied in subsequent decades until taxonomic clarification ensued in 2008. Using a recently proposed test of species delimitation, we reconfirm the phenotypic distinctness of dealbatus. We then compare three mitochondrial and seven nuclear DNA markers among 278 samples of dealbatus and alexandrinus from across their breeding range and four other closely related plovers. We fail to find any population genetic differentiation between dealbatus and alexandrinus, whereas the other species are deeply diverged at the study loci. Kentish Plovers join a small but growing list of species for which low levels of genetic differentiation are accompanied by the presence of strong phenotypic divergence, suggesting that diagnostic phenotypic characters may be encoded by few genes that are difficult to detect. Alternatively, gene expression differences may be crucial in producing different phenotypes whereas neutral differentiation may be lagging behind.

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Rheindt FE, Edwards SV. Genetic introgression: an integral but neglected component of speciation in birds. The Auk. 2011;128 :620-632. PDF
Alfoldi J, Di Palma F, Grabherr M, Williams C, Kong LS, Mauceli E, Russell P, Lowe CB, Glor RE, Jaffe JD, et al. The genome of the green anole lizard and a comparative analysis with birds and mammals. Nature. 2011;477 :587-591.Abstract

The evolution of the amniotic egg was one of the great evolutionary innovations in the history of life, freeing vertebrates from an obligatory connection to water and thus permitting the conquest of terrestrial environments(1). Among amniotes, genome sequences are available for mammals and birds(2-4), but not for non-avian reptiles. Here we report the genome sequence of the North American green anole lizard, Anolis carolinensis. We find that A. carolinensis microchromosomes are highly syntenic with chicken microchromosomes, yet do not exhibit the high GC and low repeat content that are characteristic of avian microchromosomes(2). Also, A. carolinensis mobile elements are very young and diverse-more so than in any other sequenced amniote genome. The GC content of this lizard genome is also unusual in its homogeneity, unlike the regionally variable GC content found in mammals and birds(5). We describe and assign sequence to the previously unknown A. carolinensis X chromosome. Comparative gene analysis shows that amniote egg proteins have evolved significantly more rapidly than other proteins. An anole phylogeny resolves basal branches to illuminate the history of their repeated adaptive radiations.

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Fujita MK, Edwards SV, Ponting CP. Near complete erosion of isochores in the Anolis lizard genome. Genome Biology and Evolution. 2011;3 :974-984.Abstract
Isochores are large regions of relatively homogeneous nucleotide composition and are present in the genomes of all mammals and birds that have been sequenced to date. The newly sequenced genome of Anolis carolinensis provides the first opportunity to quantify isochore structure in a nonavian reptile. We find Anolis to have the most compositionally homogeneous genome of all amniotes sequenced thus far, a homogeneity exceeding that for the frog Xenopus. Based on a Bayesian algorithm, Anolis has smaller and less GC-richisochores compared with human and chicken. Correlates generally associated with GC-rich isochores, including shorter introns and higher gene density, have all but disappeared from the Anolis genome. Using genic GC as a proxy for isochore structure so as to compare with other vertebrates, we found that GC content has substantially decreased in the lineage leading to Anolis since diverging from the common ancestor of Reptilia; 275 Ma, perhaps reflecting weakened or reversed GC-biased gene conversion, a nonadaptive substitution process that is thought to be important in the maintenance and trajectory of isochore evolution. Our results demonstrate that GC composition in Anolis is not associated with important features of genome structure, including gene density and intron size, in contrast to patterns seen in mammal and bird genomes.
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Castoe TA, Bronikowski AM, Brodie III ED, Edwards SV, Pfrender ME, Shapiro MD, Pollock DD, Warren WC. A proposal to sequence the genome of a garter snake (Thamnophis sirtalis). Standards in genomic sciences. 2011;4 :257.Abstract
Here we develop an argument in support of sequencing a garter snake (Thamnophis sirtalis) genome, and outline a plan to accomplish this. This snake is a common, widespread, nonve-nomous North American species that has served as a model for diverse studies in evolutio-nary biology, physiology, genomics, behavior and coevolution. The anole lizard is currently the only genome sequence available for a non-avian reptile. Thus, the garter snake at this time would be the first available snake genome sequence and as such would provide much needed comparative representation of non-avian reptilian genomes, and would also allow critical new in sights for vertebrate comparative genomic studies. We outline the major areas of discovery that the availability of the garter snake genome would enable, and describe a plan for whole-genome sequencing.
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