Publications

2009
Edwards S, Bensch S. Looking forwards or looking backwards in avian phylogeography? A comment on Zink and Barrowclough 2008. Molecular Ecology. 2009;18 :2930-2933.
Brito PH, Edwards SV. Multilocus phylogeography and phylogenetics using sequence-based markers. Genetica. 2009;135 :439-455.
Edwards SV. Natural selection and phylogenetic analysis. Proceedings of the National Academy of Sciences of the United States of America. 2009;106 :8799-8800.
Edwards SV. Is a new and general theory of molecular systematics emerging?. Evolution. 2009;63 :1-19.
Balakrishnan CN, Edwards SV. Nucleotide Variation, Linkage Disequilibrium and Founder-Facilitated Speciation in Wild Populations of the Zebra Finch (Taeniopygia guttata). Genetics. 2009;181 :645-660.Abstract

The zebra finch has long been an important model system for the study of vocal learning, vocal production, and behavior. With the imminent sequencing of its genome, the zebra finch is now poised to become a model system for population genetics. Using a panel of 30 noncoding loci, we characterized patterns of polymorphism and divergence among wild zebra finch populations. Continental Australian populations displayed little population structure, exceptionally high levels of nucleotide diversity (pi = 0.010), a rapid decay of linkage disequilibrium (LD), and a high population recombination rate (rho approximate to 0.05), all of which suggest an open and fluid genomic background that could facilitate adaptive variation. By contrast, Substantial divergence between the Australian and Lesser Sunda Island populations (K-ST = 0.193), reduced genetic diversity (pi = 0.002), and higher levels of LD in the island Population suggest a strong but relatively recent founder event, which may have contributed to speciation between these populations as envisioned under founder-effect speciation models. Consistent with this hypothesis, we find that tinder a simple quantitative genetic model both drift and selection could have contributed to the observed divergence in six quantitative traits. In both Australian and Lesser Sundas populations, diversity in Z-linked loci was significantly lower than in autosomal loci. Our analysis provides a quantitative framework for studying the role of selection and drift in shaping patterns of molecular evolution in the zebra finch genome.

Liu L, Edwards SV. Phylogenetic analysis in the anomaly zone. Syst Biol. 2009;58 :452-60.
Janes DE, Ezaz T, Graves JAM, Edwards SV. Recombination and nucleotide diversity in the sex chromosomal pseudoautosomal region of the Emu, Dromaius novaehollandiae. Journal of Heredity. 2009;100 :125-136.Abstract

Pseudoautosomal regions (PARs) shared by avian Z and W sex chromosomes are typically small homologous regions within which recombination still occurs and are hypothesized to share the properties of autosomes. We capitalized on the unusual structure of the sex chromosomes of emus, Dromaius novaehollandiae, which consist almost entirely of PAR shared by both sex chromosomes, to test this hypothesis. We compared recombination, linkage disequilibrium (LD), GC content, and nucleotide diversity between pseudoautosomal and autosomal loci derived from 11 emu bacterial artificial chromosome (BAC) clones that were mapped to chromosomes by fluorescent in situ hybridization. Nucleotide diversity (pi = 4N(e)mu) was not significantly lower in pseudoautosomal loci (14 loci, 1.9 +/- 2.4 x 10(-3)) than autosomal loci (8 loci, 4.2 +/- 6.1 x 10(-3)). By contrast, recombination per site within BAC-end sequences (rho = 4Nc) (pseudoautosomal, 3.9 +/- 6.9 x 10(-2); autosomal, 2.3 +/- 3.7 x 10(-2)) was higher and average LD (D') (pseudoautosomal, 4.2 +/- 0.2 x 10(-1); autosomal, 4.7 +/- 0.5 x 10(-1)) slightly lower in pseudoautosomal sequences. We also report evidence of deviation from a simple neutral model in the PAR and in autosomal loci, possibly caused by departures from demographic equilibrium, such as population growth. This study provides a snapshot of the population genetics of avian sex chromosomes at an early stage of differentiation.

Claessens LP, Edwards SV, Martinez R, Krzyzak M, Eckardt M, Leslie G, Marcucci M, Neabore S, Vrcek I, Moss S, et al. Aves 3D: A new online resource for avian skeletal anatomy. Integrative and Comparative Biology [Internet]. 2009;49 :E213-E213. Publisher's VersionAbstract
P2.108
CLAESSENS, L.P.*; EDWARDS, S.V.; MARTINEZ, R.; KRZYZAK,
M.; ECKARDT, M.; LESLIE, G.; MARCUCCI, M.; NEABORE, S.; VRCEK, I.;
MOSS, S.; GRASSI, K.; College of the Holy Cross, Worcester, MA, Harvard
University, Cambridge, MA;
Aves 3D: A new online resource for avian skeletal anatomy
Here we report the launch of a new National Science Foundation funded
online resource for avian skeletal anatomy, www.Aves3D.org, which will offer
three-dimensional models of a wide selection of skeletal elements of extant
and extinct birds. The Aves 3D database is produced through non-contact
laser scanning of skeletal material from, amongst others, the Harvard
Museum of Comparative Zoology and the Yale Peabody Museum of Natural
History. Database growth is fueled by undergraduate student research
projects, which involve a variety of functional and phylogenetic studies
supervised by both affiliated and external post-graduate students and
researchers. The online database will also serve as a digital archive for the
collections of contributing museums and allows for rapid global dissemination
of 3D digital data on common as well as rare and potentially fragile
specimens, in a format ready for a wide range of two and three-dimensional
computational analyses. The size of the database is currently limited, and
opportunities exist for initiating new student-based projects that will

contribute to database growth

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Chapus C, Edwards SV. Genome evolution in Reptilia: in silico chicken mapping of 12,000 BAC-end sequences from two reptiles and a basal bird. Bmc Genomics [Internet]. 2009;10. Publisher's VersionAbstract

Background

With the publication of the draft chicken genome and the recent production of several BAC clone libraries from non-avian reptiles and birds, it is now possible to undertake more detailed comparative genomic studies in Reptilia. Of interest in particular are the genomic events that transformed the large, repeat-rich genomes of mammals and non-avian reptiles into the minimalist chicken genome. We have used paired BAC end sequences (BESs) from the American alligator (Alligator mississippiensis), painted turtle (Chrysemys picta) and emu (Dromaius novaehollandiae) to investigate patterns of sequence divergence, gene and retroelement content, and microsynteny between these species and chicken.

Results

From a total of 11,967 curated BESs, we successfully mapped 725, 773 and 2597 sequences in alligator, turtle, and emu, respectively, to sites in the draft chicken genome using a stringent BLAST protocol. Most commonly, sequences mapped to a single site in the chicken genome. Of 1675, 1828 and 2936 paired BESs obtained for alligator, turtle, and emu, respectively, a total of 34 (alligator, 2%), 24 (turtle, 1.3%) and 479 (emu, 16.3%) pairs were found to map with high confidence and in the correct orientation and with BAC-sized intermarker distances to single chicken chromosomes, including 25 such paired hits in emu mapping to the chicken Z chromosome. By determining the insert sizes of a subset of BAC clones from these three species, we also found a significant correlation between the intermarker distance in alligator and turtle and in chicken, with slopes as expected on the basis of the ratio of the genome sizes.

Conclusion

Our results suggest that a large number of small-scale chromosomal rearrangements and deletions in the lineage leading to chicken have drastically reduced the number of detected syntenies observed between the chicken and alligator, turtle, and emu genomes and imply that small deletions occurring widely throughout the genomes of reptilian and avian ancestors led to the ~50% reduction in genome size observed in birds compared to reptiles. We have also mapped and identified likely gene regions in hundreds of new BAC clones from these species.

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Janes DE, Organ CL, Edwards SV. Variability in Sex-Determining Mechanisms Influences Genome Complexity in Reptilia. Cytogenetic and Genome Research [Internet]. 2009;127 (2-4) :242-248. Publisher's VersionAbstract

In this review, we describe the history of amniote sex determination as a classic example of Darwinian evolution. We suggest that evolutionary changes in sex determination provide a foundation for understanding important aspects of chromosome and genome organization that otherwise appear haphazard in their origins and contents. Species with genotypic sex determination often possess heteromorphic sex chromosomes, whereas species with environmental sex determination lack them. Through a series of mutations followed by selection at key genes, sex-determining mechanisms have turned over many times throughout the amniote lineage. As a consequence, amniote genomes have undergone gains or losses of sex chromosomes. We review the genomic and ecological contexts in which either temperature-dependent or genotypic sex determination has evolved. Once genotypic sex determination emerges in a lineage, viviparity and heteromorphic sex chromosomes become more likely to evolve. For example, in extinct marine reptiles, genotypic sex determination apparently led to viviparity, which in turn facilitated their pelagic radiation. Sex chromosomes comprise genome regions that differ from autosomes in recombination rate, mutation rate, levels of polymorphism, and the presence of sex-determining and sexually antagonistic genes. In short, many aspects of amniote genome complexity, life history, and adaptive radiation appear contingent on evolutionary changes in sex-determining mechanisms.

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2008
Janes DE, Ezaz T, Graves JAM, Edwards SV. Characterization, chromosomal location, and genomic neighborhood of a ratite ortholog of a gene with gonadal expression in mammals. Integrative and Comparative Biology. 2008;48 :505-511.Abstract

A locus that we name SubA was discovered during large-scale sequencing and characterization of a bacterial artificial chromosome library from an emu, Dromaius novaehollandiae. This locus yields a significantly negative Tajimas D in emus and is conserved across emu, chicken, mouse, and human. Expression of SubA orthologs has been reported in human ovaries and in mouse testes, but remains unknown in emus. The locus was physically mapped onto a pair of microchromosomes in emus by fluorescent in situ hybridization and also in chicken as previously reported. By characterizing emu SubA in this article, we aim to improve current descriptions of the cascade of genes associated with avian sex differentiation. Future experimentation will report the expression of SubA in ratites, other birds, and nonavian reptiles.

Brumfield RT, Liu L, Lum DE, Edwards SV. Comparison of Species Tree Methods for Reconstructing the Phylogeny of Bearded Manakins (Aves: Pipridae, Manacus) from Multilocus Sequence Data. Systematic Biology. 2008;57 :719-731.Abstract

Although the power of multi-locus data in estimating species trees is apparent, it is also clear that the analytical methodologies for doing so are still maturing. For example, of the methods currently available for estimating species trees from multiocus data, the Bayesian method introduced by Liu and Pearl (2007; BEST) is the only one that provides nodal support values. Using gene sequences from five nuclear loci, we explored two analytical methods (deep coalescence and BEST) to reconstruct the species tree of the five primary Manacus OTUs: M. aurantiacus, M. candei, M. vitellinus, populations of M. manacus from west of the Andes (M. manacus (w)), and populations of M. manacus from east of the Andes (M. manacus (e)). Both BEST and deep coalescence supported a sister relationship between M. vitellinus and M. manacus (w). A lower probability tree from the BEST analysis and one of the most parsimonious deep coalescence trees also supported a sister relationship between M. candei and M. aurantiacus. Because hybrid zones connect the distributions of most Manacus species, we examined the potential influence of post-divergence gene flow on the sister relationship of parapatrically distributed M. vitellinus and M. manacus (w). An isolation-with-migration (IM) analysis found relatively high levels of gene flow between M. vitellinus and M. manacus (w). Whether the gene flow is obscuring a true sister relationship between M. manacus (w) and M. manacus (e) remained unclear, pointing to the need for more detailed models accommodating multispecies, multilocus DNA sequence data.

Thomson RC, Shedlock AM, Edwards SV, Shaffer HB. Developing markers for multilocus phylogenetics in non-model organisms: a test case with turtles. Molecular Phylogenetics and Evolution. 2008;49 :514-525.
Lee JY, Edwards SV. Divergence across Australia's Carpentarian Barrier: Statistical Phylogeography of the Red-Backed Fairy Wren(Malurus Melanocephalus). Evolution. 2008;62 :3117-3134.Abstract

Multilocus analysis of phylogeography and population history is a powerful tool for understanding the origin, dispersal, and geographic structure of species over time and space. Using 36 genetic markers (29 newly developed anonymous nuclear loci, six introns and one from mitochondrial DNA, amounting to over 15 kb per individual), we studied population structure and demographic history of the red-backed fairy wren Malurus melanocephalus, a small passerine distributed in the northern and eastern part of Australia across the Carpentarian barrier. Analysis of anonymous loci markers revealed large amounts of genetic diversity (pi = 0.016 +/- 0.01; average number of SNPs per locus = 48; total number of SNPs = 1395), and neither nuclear nor mitochondrial gene trees showed evidence of reciprocal monophyly among Cape York (CY), Eastern Forest (EF), and Top End (TE) populations. Despite traditional taxonomy linking TE and CY populations to the exclusion of EF, we found that the CY population is genetically closer to the EF population, consistent with predicted area cladograms in this region. Multilocus coalescent analysis suggests that the CY population was separated from the other two regions approximately 0.27 million years ago, and that significant gene flow between the ER and the CY populations (similar to 2 migrants per generation) suggests geographic continuity in eastern Australia. By contrast, gene flow between the CY and the TE populations has been dampened by divergence across the Carpentarian barrier.

Bonneaud C, Burnside J, Edwards SV. High-speed developments in avian genomics. Bioscience. 2008;58 :587-595.
Organ CL, Moreno RG, Edwards SV. Three tiers of genome evolution in reptiles. Integrative and Comparative Biology. 2008;48 :494-504.Abstract

Characterization of reptilian genomes is essential for understanding the overall diversity and evolution of amniote genomes, because reptiles, which include birds, constitute a major fraction of the amniote evolutionary tree. To better understand the evolution and diversity of genomic characteristics in Reptilia, we conducted comparative analyses of online sequence data from Alligator mississippiensis (alligator) and Sphenodon punctatus (tuatara) as well as genome size and karyological data from a wide range of reptilian species. At the whole-genome and chromosomal tiers of organization, we find that reptilian genome size distribution is consistent with a model of continuous gradual evolution while genomic compartmentalization, as manifested in the number of microchromosomes and macrochromosomes, appears to have undergone early rapid change. At the sequence level, the third genomic tier, we find that exon size in Alligator is distributed in a pattern matching that of exons in Gallus (chicken), especially in the 101200 bp size class. A small spike in the fraction of exons in the 301 bp1 kb size class is also observed for Alligator, but more so for Sphenodon. For introns, we find that members of Reptilia have a larger fraction of introns within the 101 bp2 kb size class and a lower fraction of introns within the 530 kb size class than do mammals. These findings suggest that the mode of reptilian genome evolution varies across three hierarchical levels of the genome, a pattern consistent with a mosaic model of genomic evolution.

Causey D, Edwards SV. Ecology of avian influenza virus in birds. Journal of Infectious Diseases [Internet]. 2008;197 :S29-S33. Publisher's VersionAbstract

Avian influenza A virus (an orthomyxovirus) is a zoonotic pathogen with a natural reservoir entirely in birds. The influenza virus genome is an 8-segment single-stranded RNA with high potential for in situ recombination. Two segments code for the hemagglutinin (H) and neuraminidase (N) antigens used for host-cell entry. At present, 16 H and 9 N subtypes are known, for a total of 144 possible different influenza subtypes, each with potentially different host susceptibility. With >10,000 species of birds found in nearly every terrestrial and aquatic habitat, there are few places on earth where birds cannot be found. The avian immune system differs from that of humans in several important features, including asynchronous B and T lymphocyte systems and a polymorphic multigene immune complex, but little is known about the immunogenetics of pathogenic response. Postbreeding dispersal and migration and a naturally high degree of environmental vagility mean that wild birds have the potential to be vectors that transmit highly pathogenic variants great distances from the original sources of infection.

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Liu L, Pearl DK, Brumfield RT, Edwards SV. Estimating species trees using multiple-allele DNA sequence data. Evolution [Internet]. 2008;62 (8) :2080-2091. Publisher's VersionAbstract
Several techniques, such as concatenation and consensus methods, are available for combining data from multiple loci to produce
a single statement of phylogenetic relationships. However, when multiple alleles are sampled from individual species, it becomes
more challenging to estimate relationships at the level of species, either because concatenation becomes inappropriate due to
conflicts among individual gene trees, or because the species from which multiple alleles have been sampled may not form
monophyletic groups in the estimated tree. We propose a Bayesian hierarchical model to reconstruct species trees from multiple-
allele, multilocus sequence data, building on a recently proposed method for estimating species trees from single allele multilocus
data. A two-step Markov Chain Monte Carlo (MCMC) algorithm is adopted to estimate the posterior distribution of the species tree.
The model is applied to estimate the posterior distribution of species trees for two multiple-allele datasets—yeast (
Saccharomyces
)
and birds (
Manacus
—manakins). The estimates of the species trees using our method are consistent with those inferred from other
methods and genetic markers, but in contrast to other species tree methods, it provides credible regions for the species tree. The
Bayesian approach described here provides a powerful framework for statistical testing and integration of population genetics
and phylogenetics.
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Limaye N, Belobrajdic KA, Wandstrat AE, Bonhomme F, Edwards SV, Wakeland EK. Prevalence and evolutionary origins of autoimmune susceptibility alleles in natural mouse populations. Genes and Immunity [Internet]. 2008;9 (1) :61-68. Publisher's VersionAbstract
The evolutionary origin of genetic diversity in the SLAM/CD2 gene cluster, implicated in autoimmune lupus susceptibility in
mice, was investigated by sequence analysis of exons from six members of the cluster in 48 wild mouse samples derived from
the global mouse population. A total of 80 coding region SNPs were identified among the six genes analyzed, indicating that
this gene cluster is highly polymorphic in natural mouse populations. Phylogenetic analyses of these allelic sequences revealed
clustering of alleles derived from multiple Mus species and subspecies, indicating alleles at several SLAM/CD2 loci were
present in ancestral Mus populations prior to speciation and have persisted as polymorphisms for more than 1 million years.
Analyses of nonsynonymous/synonymous ratios using likelihood codon substitution models identified several segments in
Cd229, Cd48 and Cd84 that were impacted by positive diversifying selective pressures. These findings support
the interpretation that selection favoring the generation and retention of functional polymorphisms has played a role in the
evolutionary origin of genetic polymorphisms that are predisposing to autoimmunity.
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2007
Edwards SV, Liu L, Pearl DK. High-resolution species trees without concatenation. Proceedings of the National Academy of Sciences of the United States of AmericaProceedings of the National Academy of Sciences of the United States of America. 2007;104 :5936-41.Abstract
The vast majority of phylogenetic models focus on resolution of gene trees, despite the fact that phylogenies of species in which gene trees are embedded are of primary interest. We analyze a Bayesian model for estimating species trees that accounts for the stochastic variation expected for gene trees from multiple unlinked loci sampled from a single species history after a coalescent process. Application of the model to a 106-gene data set from yeast shows that the set of gene trees recovered by statistically acknowledging the shared but unknown species tree from which gene trees are sampled is much reduced compared with treating the history of each locus independently of an overarching species tree. The analysis also yields a concentrated posterior distribution of the yeast species tree whose mode is congruent with the concatenated gene tree but can do so with less than half the loci required by the concatenation method. Using simulations, we show that, with large numbers of loci, highly resolved species trees can be estimated under conditions in which concatenation of sequence data will positively mislead phylogeny, and when the proportion of gene trees matching the species tree is <10%. However, when gene tree/species tree congruence is high, species trees can be resolved with just two or three loci. These results make accessible an alternative paradigm for combining data in phylogenomics that focuses attention on the singularity of species histories and away from the idiosyncrasies and multiplicities of individual gene histories.

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