Publications

2013
Bradley Shaffer H, Minx P, Warren D, Shedlock A, Thomson R, Valenzuela N, Abramyan J, Amemiya C, Badenhorst D, Biggar K, et al. The western painted turtle genome, a model for the evolution of extreme physiological adaptations in a slowly evolving lineage. Genome Biology. 2013;14 :R28.Abstract

BACKGROUND:We describe the genome of the western painted turtle, Chrysemys picta bellii, one of the most widespread, abundant, and well-studied turtles. We place the genome into a comparative evolutionary context, and focus on genomic features associated with tooth loss, immune function, longevity, sex differentiation and determination, and the species' physiological capacities to withstand extreme anoxia and tissue freezing.RESULTS:Our phylogenetic analyses confirm that turtles are the sister group to living archosaurs, and demonstrate an extraordinarily slow rate of sequence evolution in the painted turtle. The ability of the painted turtle to withstand complete anoxia and partial freezing appears to be associated with common vertebrate gene networks, and we identify candidate genes for future functional analyses. Tooth loss shares a common pattern of pseudogenization and degradation of tooth-specific genes with birds, although the rate of accumulation of mutations is much slower in the painted turtle. Genes associated with sex differentiation generally reflect phylogeny rather than convergence in sex determination functionality. Among gene families that demonstrate exceptional expansions or show signatures of strong natural selection, immune function and musculoskeletal patterning genes are consistently over-represented.CONCLUSIONS:Our comparative genomic analyses indicate that common vertebrate regulatory networks, some of which have analogs in human diseases, are often involved in the western painted turtle's extraordinary physiological capacities. As these regulatory pathways are analyzed at the functional level, the painted turtle may offer important insights into the management of a number of human health disorders.

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Backstroem N, Shipilina D, Blom MPK, Edwards SV. Cis-regulatory sequence variation and association with Mycoplasma load in natural populations of the house finch (Carpodacus mexicanus). Ecology and Evolution [Internet]. 2013;3 (3) :655-666. Publisher's VersionAbstract
Characterization of the genetic basis of fitness traits in natural populations is
important for understanding how organisms adapt to the changing environ-
ment and to novel events, such as epizootics. However, candidate fitness-
influencing loci, such as regulatory regions, are usually unavailable in nonmodel
species. Here, we analyze sequence data from targeted resequencing of the cis-
regulatory regions of three candidate genes for disease resistance (CD74,
HSP90a, and LCP1) in populations of the house finch (Carpodacus mexicanus)
historically exposed (Alabama) and na
ıve (Arizona) to Mycoplasma gallisepti-
cum. Our study, the first to quantify variation in regulatory regions in wild
birds, reveals that the upstream regions of CD74 and HSP90a are GC-rich, with
the former exhibiting unusually low sequence variation for this species. We
identified two SNPs, located in a GC-rich region immediately upstream of an
inferred promoter site in the gene HSP90a, that were significantly associated
with Mycoplasma pathogen load in the two populations. The SNPs are closely
linked and situated in potential regulatory sequences: one in a binding site for
the transcription factor nuclear NFYa and the other in a dinucleotide microsat-
ellite ((GC)
6
). The genotype associated with pathogen load in the putative
NFYa binding site was significantly overrepresented in the Alabama birds.
However, we did not see strong effects of selection at this SNP, perhaps because
selection has acted on standing genetic variation over an extremely short time
in a highly recombining region. Our study is a useful starting point to explore
functional relationships between sequence polymorphisms, gene expression, and
phenotypic traits, such as pathogen resistance that affect fitness in the wild.
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Backstroem N, Zhang Q, Edwards SV. Evidence from a House Finch (Haemorhous mexicanus) Spleen Transcriptome for Adaptive Evolution and Biased Gene Conversion in Passerine Birds. Molecular Biology and Evolution [Internet]. 2013;30 (5) :1046-1050. Publisher's VersionAbstract
Identifying genes influenced by natural selection can provid
e information about lineage-specific adaptations, and tran-
scriptomes generated by next-generation sequencing are a us
eful resource for identifying such genes. Here, we utilize a
spleen transcriptome for the house finch (
Haemorhous mexicanus
), an emerging model for sexual selection and disease
ecology, together with previously sequenced avian geno
mes (chicken, turkey, and zebra finch), to investigate
lineage-specific adaptations within birds. An analysis of 4,
398 orthologous genes revealed a significantly higher ratio
of nonsynonymous to synonymous substit
utions and significantly higher GC content in passerines than in galliforms, an
observation deviating from strictly neutral expectations b
ut consistent with an effect of biased gene conversion on the
evolutionary rate in passerines. These data also showed that ge
nes exhibiting signs of positive selection and fast evolution
in passerines have functional roles related to fat m
etabolism, neurodevelopment, and ion binding.
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do Amaral FR, Albers PK, Edwards SV, Miyaki CY. Multilocus tests of Pleistocene refugia and ancient divergence in a pair of Atlantic Forest antbirds (Myrmeciza). Molecular Ecology [Internet]. 2013;22 (15) :3996-4013. Publisher's VersionAbstract
The Atlantic Forest (AF) harbours one of the most diverse vertebrate faunas of the
world, including 199 endemic species of birds. Understanding the evolutionary pro-
cesses behind such diversity has become the focus of many recent, primarily single
locus, phylogeographic studies. These studies suggest that isolation in forest refugia
may have been a major mechanism promoting diversification, although there is also
support for a role of riverine and geotectonic barriers, two sets of hypotheses that can
best be tested with multilocus data. Here we combined multilocus data (one mtDNA
marker and eight anonymous nuclear loci) from two species of parapatric antbirds,
Myrmeciza loricata
and
M. squamosa
, and Approximate Bayesian Computation to
determine whether isolation in refugia explains current patterns of genetic variation
and their status as independent evolutionary units. Patterns of population structure,
differences in intraspecific levels of divergence and coalescent estimates of historical
demography fit the predictions of a recently proposed model of refuge isolation in
which climatic stability in the northern AF sustains higher diversity and demographic
stability than in the southern AF. However, a pre-Pleistocene divergence associated
with their abutting range limits in a region of past tectonic activity also suggests a role
for rivers or geotectonic barriers. Little or no gene flow between these species suggests
the development of reproductive barriers or competitive exclusion. Our results sug-
gests that limited marker sampling in recent AF studies may compromise estimates of
divergence times and historical demography, and we discuss the effects of such sam-
pling on this and other studies.
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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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