Publications

2015
Edwards SV, Schultz A, Campbell-Staton S. Next-generation sequencing and the expanding domain of phylogeography. Folia Zoologica. 2015;64 :187-206.Abstract

Phylogeography is experiencing a revolution brought on by next-generation sequencing methods. A historical survey of the
phylogeographic literature suggests that phylogeography typically incorporates new questions, expanding on its classical domain, when new
technologies offer novel or increased numbers of molecular markers. A variety of methods for subsampling genomic variation, including
restriction site associated DNA sequencing (Rad-seq) and other next generation approaches, are proving exceptionally useful in helping
to define major phylogeographic lineages within species as well as details of historical demography. Next-generation methods are also
blurring the edges of phylogeography and related fields such as association mapping of loci under selection, and the emerging paradigm
is one of simultaneously inferring both population history across geography and genomic targets of selection. However, recent examples,
including some from our lab on Anolis lizards and songbirds, suggest that genome subsampling methods, while extremely powerful for the
classical goals of phylogeography, may fail to allow phylogeography to fully achieve the goals of this new, expanded domain. Specifically,
if genome-wide linkage disequilibrium is low, as is the case in many species with large population sizes, most genome subsampling
methods will not sample densely enough to detect selected variants, or variants closely linked to them. We suggest that whole-genome
resequencing methods will be essential for allowing phylogeographers to robustly identify loci involved in phenotypic divergence and
speciation, while at the same time allowing free choice of molecular markers and further resolution of the demographic history of species.

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Badenhorst D, Hillier LDW, Literman R, Montiel EE, Radhakrishnan S, Shen Y, Minx P, Janes DE, Warren WC, Edwards SV, et al. Physical Mapping and Refinement of the Painted Turtle Genome ( Chrysemys picta ) Inform Amniote Genome Evolution and Challenge Turtle-Bird Chromosomal Conservation. Genome Biology and Evolution. 2015;7 :2038-2050.Abstract
Comparative genomics continues illuminating amniote genome evolution, but for man
y lineages our understanding remains incom-plete. Here, we refine the assembly (CPI 3.0.3 NCBI AHGY00000000.2) and develop a cytogenetic map of the painted turtle (Chrysemyspicta—CPI) genome, the first in turtles and in vertebrates with temperature-dependent sex determination. A comparison of turtle genomes with those of chicken, selected nonavian reptiles, and human revealed shared and novel genomic features, such as numerous chromosomal rearrangements. The largest conserved syntenic blocks between birds and turtles exist in four macrochro-mosomes, whereas rearrangements were evident in these and other chromosomes, disproving that turtles and birds retain fully
conserved macrochromosomes for greater than 300 Myr. C-banding re
vealed large heterochromatic blocks in the centromeric region
of only few chromosomes. The nucleolar-org
anizing region (NOR) mapped to a single CPI microchromosome, whereas in some turtles
and lizards the NOR maps to nonhomologous sex-chromosomes, t
hus revealing independent translocations of the NOR in various reptilian lineages. There was no evidence for recent chromosomal fusions as interstitial telomeric-DNA was absent. Some repeat elements (CR1-like, Gypsy) were enriched in the centromere s of five chromosomes, whereas others were widespread in the CPI
genome. Bacterial artificial chromosome (BAC) clones were hybridized to 18 of the 25 CPI chromosomes and anchored to a G-banded ideogram. Several CPI sex-determining genes mapped to five ch romosomes, and homology was detected between yet other CPI autosomes and the globally nonhomologous sex chromosomes of chicken, other turtles, and squamates, underscoring the inde-pendent evolution of vertebrate sex-determining mechanisms.
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Lowe CB, Clarke JA, Baker AJ, Haussler D, Edwards SV. Feather Development Genes and Associated Regulatory Innovation Predate the Origin of Dinosauria. Molecular Biology and Evolution [Internet]. 2015;32 (1) :23-28. Publisher's VersionAbstract
The evolution of avian feathers have recently been illuminated by fossils and the
identification of genes involved in feather patterning and morphogenesis.
However, molecular studies have focused mainly on protein-coding genes.
Using comparative genomics and more than 600,000 conserved regulatory
elements, we show that patterns of genome evolution in the vicinity of feather genes
are consistent with a major role for regulatory innovation in the evolution of feathers. Rates
of innovation at feather regulatory elements exhibit an extended period of innovation with peaks in the ancestors of amniotes and archosaurs. We estimate that 86% of such regulatory elements were present prior to the origin of Dinosauria. On the branch leading to modern birds, we detect a strong signal of regulatory innovation near IGFB P2 and IGFBP5, which have roles in body size reduction, and may represent a genomic signature for the miniaturization of dinosaurian body size preceding the origin of flight.
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Balenger SL, Bonneaud C, Sefick SA, Edwards SV, Hill GE. Plumage color and pathogen-induced gene expression in a wild bird. Behavioral Ecology [Internet]. 2015;26 (4) :1100-1110. Publisher's Version PDF
2014
Zhang GJ, Li C, Li QY, Li B, Larkin DM, Lee C, Storz JF, Antunes A, Greenwold MJ, Meredith RW, et al. Comparative genomics reveals insights into avian genome evolution and adaptation. Science. 2014;346 :1311-1320.Abstract

Birds are the most species-rich class of tetrapod vertebrates and have wide relevance across many research fields. We explored bird macroevolution using full genomes from 48 avian species representing all major extant clades. The avian genome is principally characterized by its constrained size, which predominantly arose because of lineage-specific erosion of repetitive elements, large segmental deletions, and gene loss. Avian genomes furthermore show a remarkably high degree of evolutionary stasis at the levels of nucleotide sequence, gene synteny, and chromosomal structure. Despite this pattern of conservation, we detected many non-neutral evolutionary changes in protein-coding genes and noncoding regions. These analyses reveal that pan-avian genomic diversity covaries with adaptations to different lifestyles and convergent evolution of traits.

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Wu SY, Zhang FC, Edwards SV, Wu WY, Ye J, Bi SD, Ni XJ, Quan C, Meng J, Organ CL. The Evolution of Bipedalism in Jerboas (Rodentia: Dipodoidea): Origin in Humid and Forested Environments. Evolution. 2014;68 :2108-2118.Abstract

Mammalian bipedalism has long been thought to have arisen in response to arid and open environments. Here, we tested whether bipedalism coevolved with environmental changes using molecular and paleontological data from the rodent superfamily Dipodoidea and statistical methods for reconstructing ancestral characteristics and past climates. Our results show that the post-Late Miocene aridification exerted selective pressures on tooth shape, but not on leg length of bipedal jerboas. Cheek tooth crown height has increased since the Late Miocene, but the hind limb/head-body length ratios remained stable and high despite the environmental change from humid and forested to arid and open conditions, rather than increasing from low to high as predicted by the arid-bipedalism hypothesis. The decoupling of locomotor and dental character evolution indicates that bipedalism evolved under selective pressure different from that of dental hypsodonty in jerboas. We reconstructed the habitats of early jerboas using floral and faunal data, and the results show that the environments in which bipedalism evolved were forested. Our results suggest that bipedalism evolved as an adaptation to humid woodlands or forests for vertical jumping. Running at high speeds is likely a by-product of selection for jumping, which became advantageous in open environments later on.

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Lowe CB, Clarke JA, Baker AJ, Haussler D, Edwards SV. Feather development genes and associated regulatory innovation predate the origin of Dinosauria. Molecular Biology and Evolution. 2014;32 :23-28.Abstract
The evolution of avian feathers has recently been illumin
ated by fossils and the identification of genes involved in
feather patterning and morphogenesis. However, molecula
r studies have focused mainly on protein-coding genes.
Using comparative genomics and more than 600,000 conserved regulatory elements, we show that patterns of genome evolution in the vicinity of feather genes are consistent with a major role for regulatory innovation in the evolution of feathers. Rates of innovation at feather regulatory elements exhibit an extended period of innovation with peaks in the ancestors of amniotes and archosaurs. We estimate that 86% of such regulatory elements and 100% of the nonkeratin feather gene set were present prior to the origin of Dinosauria. On the branch leading to modern birds, we detect a strong signal of regulatory innovation near insulin-like growth factor binding protein (IGFBP) 2 and IGFBP5, which have roles in body size reduction, and may represent a genomic signature for the miniaturization of dinosaurian body size preceding the origin of flight.
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Zhang Q, Hill GE, Edwards SV, Backström N. A house finch (Haemorhous mexicanus) spleen transcriptome reveals intra- and interspecific patterns of gene expression, alternative splicing and genetic diversity in passerines. Bmc Genomics. 2014;15 :305-305.Abstract

BACKGROUND: With its plumage color dimorphism and unique history in North America, including a recent population expansion and an epizootic of Mycoplasma gallisepticum (MG), the house finch (Haemorhous mexicanus) is a model species for studying sexual selection, plumage coloration and host-parasite interactions. As part of our ongoing efforts to make available genomic resources for this species, here we report a transcriptome assembly derived from genes expressed in spleen. RESULTS: We characterize transcriptomes from two populations with different histories of demography and disease exposure: a recently founded population in the eastern US that has been exposed to MG for over a decade and a native population from the western range that has never been exposed to MG. We utilize this resource to quantify conservation in gene expression in passerine birds over approximately 50 MY by comparing splenic expression profiles for 9,646 house finch transcripts and those from zebra finch and find that less than half of all genes expressed in spleen in either species are expressed in both species. Comparative gene annotations from several vertebrate species suggest that the house finch transcriptomes contain ~15 genes not yet found in previously sequenced vertebrate genomes. The house finch transcriptomes harbour ~85,000 SNPs, ~20,000 of which are non-synonymous. Although not yet validated by biological or technical replication, we identify a set of genes exhibiting differences between populations in gene expression (n = 182; 2% of all transcripts), allele frequencies (76 FST ouliers) and alternative splicing as well as genes with several fixed non-synonymous substitutions; this set includes genes with functions related to double-strand break repair and immune response. CONCLUSIONS: The two house finch spleen transcriptome profiles will add to the increasing data on genome and transcriptome sequence information from natural populations. Differences in splenic expression between house finch and zebra finch imply either significant evolutionary turnover of splenic expression patterns or different physiological states of the individuals examined. The transcriptome resource will enhance the potential to annotate an eventual house finch genome, and the set of gene-based high-quality SNPs will help clarify the genetic underpinnings of host-pathogen interactions and sexual selection.

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Janes DE, Organ CL, Stiglec R, O'Meally D, Sarre SD, Georges A, Graves JA, Valenzuela N, Literman RA, Rutherford K, et al. Molecular evolution of Dmrt1 accompanies change of sex-determining mechanisms in reptilia. Biology Letters. 2014;10.Abstract

In reptiles, sex-determining mechanisms have evolved repeatedly and reversibly between genotypic and temperature-dependent sex determination. The gene Dmrt1 directs male determination in chicken (and presumably other birds), and regulates sex differentiation in animals as distantly related as fruit flies, nematodes and humans. Here, we show a consistent molecular difference in Dmrt1 between reptiles with genotypic and temperature-dependent sex determination. Among 34 non-avian reptiles, a convergently evolved pair of amino acids encoded by sequence within exon 2 near the DM-binding domain of Dmrt1 distinguishes species with either type of sex determination. We suggest that this amino acid shift accompanied the evolution of genotypic sex determination from an ancestral condition of temperature-dependent sex determination at least three times among reptiles, as evident in turtles, birds and squamates. This novel hypothesis describes the evolution of sex-determining mechanisms as turnover events accompanied by one or two small mutations.

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Cook JA, Edwards SV, Lacey EA, Guralnick RP, Soltis PS, Soltis DE, Welch CK, Bell KC, Galbreath KE, Himes C, et al. Natural History Collections as Emerging Resources for Innovative Education. Bioscience. 2014;64 :725-734.Abstract

There is an emerging consensus that undergraduate biology education in the United States is at a crucial juncture, especially as we acknowledge the need to train a new generation of scientists to meet looming environmental and health crises. Digital resources for biology now available online provide an opportunity to transform biology curricula to include more authentic and inquiry-driven educational experiences. Digitized natural history collections have become tremendous assets for research in environmental and health sciences, but, to date, these data remain largely untapped by educators. Natural history collections have the potential to help transform undergraduate science education from passive learning into an active exploration of the natural world, including the exploration of the complex relationships among environmental conditions, biodiversity, and human well-being. By incorporating natural history specimens and their associated data into undergraduate curricula, educators can promote participatory learning and foster an understanding of essential interactions between organisms and their environments.

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McGlothlin JW, Chuckalovcak JP, Janes DE, Edwards SV, Feldman CR, Brodie ED, Pfrender ME, Brodie ED. Parallel Evolution of Tetrodotoxin Resistance in Three Voltage-Gated Sodium Channel Genes in the Garter Snake Thamnophis sirtalis. Molecular Biology and Evolution. 2014.Abstract

Members of a gene family expressed in a single species often experience common selection pressures. Consequently, the molecular basis of complex adaptations may be expected to involve parallel evolutionary changes in multiple paralogs. Here, we use bacterial artificial chromosome library scans to investigate the evolution of the voltage-gated sodium channel (Nav) family in the garter snake Thamnophis sirtalis, a predator of highly toxic Taricha newts. Newts possess tetrodotoxin (TTX), which blocks Nav’s, arresting action potentials in nerves and muscle. Some Thamnophis populations have evolved resistance to extremely high levels of TTX. Previous work has identified amino acid sites in the skeletal muscle sodium channel Nav1.4 that confer resistance to TTX and vary across populations. We identify parallel evolution of TTX resistance in two additional Nav paralogs, Nav1.6 and 1.7, which are known to be expressed in the peripheral nervous system and should thus be exposed to ingested TTX. Each paralog contains at least one TTX-resistant substitution identical to a substitution previously identified in Nav1.4. These sites are fixed across populations, suggesting that the resistant peripheral nerves antedate resistant muscle. In contrast, three sodium channels expressed solely in the central nervous system (Nav1.1–1.3) showed no evidence of TTX resistance, consistent with protection from toxins by the blood–brain barrier. We also report the exon–intron structure of six Nav paralogs, the first such analysis for snake genes. Our results demonstrate that the molecular basis of adaptation may be both repeatable across members of a gene family and predictable based on functional considerations.

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Baldwin MW, Toda Y, Nakagita T, O'Connell MJ, Klasing KC, Misaka T, Edwards SV, Liberles SD. Sensory biology. Evolution of sweet taste perception in hummingbirds by transformation of the ancestral umami receptor. Science (New York, N.Y.). 2014;345 :929-33.Abstract

Sensory systems define an animal's capacity for perception and can evolve to promote survival in new environmental niches. We have uncovered a noncanonical mechanism for sweet taste perception that evolved in hummingbirds since their divergence from insectivorous swifts, their closest relatives. We observed the widespread absence in birds of an essential subunit (T1R2) of the only known vertebrate sweet receptor, raising questions about how specialized nectar feeders such as hummingbirds sense sugars. Receptor expression studies revealed that the ancestral umami receptor (the T1R1-T1R3 heterodimer) was repurposed in hummingbirds to function as a carbohydrate receptor. Furthermore, the molecular recognition properties of T1R1-T1R3 guided taste behavior in captive and wild hummingbirds. We propose that changing taste receptor function enabled hummingbirds to perceive and use nectar, facilitating the massive radiation of hummingbird species.

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Green RE, Braun EL, Armstrong J, Earl D, Nguyen N, Hickey G, Vandewege MW, St John JA, Capella-Gutierrez S, Castoe TA, et al. Three crocodilian genomes reveal ancestral patterns of evolution among archosaurs. Science. 2014;346 :1335-+.Abstract

To provide context for the diversification of archosaurs-the group that includes crocodilians, dinosaurs, and birds-we generated draft genomes of three crocodilians: Alligator mississippiensis (the American alligator), Crocodylus porosus (the saltwater crocodile), and Gavialis gangeticus (the Indian gharial). We observed an exceptionally slow rate of genome evolution within crocodilians at all levels, including nucleotide substitutions, indels, transposable element content and movement, gene family evolution, and chromosomal synteny. When placed within the context of related taxa including birds and turtles, this suggests that the common ancestor of all of these taxa also exhibited slow genome evolution and that the comparatively rapid evolution is derived in birds. The data also provided the opportunity to analyze heterozygosity in crocodilians, which indicates a likely reduction in population size for all three taxa through the Pleistocene. Finally, these data combined with newly published bird genomes allowed us to reconstruct the partial genome of the common ancestor of archosaurs, thereby providing a tool to investigate the genetic starting material of crocodilians, birds, and dinosaurs.

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Jarvis ED, Mirarab S, Aberer AJ, Li B, Houde P, Li C, Ho SYW, Faircloth BC, Nabholz B, Howard JT, et al. Whole-genome analyses resolve early branches in the tree of life of modern birds. Science. 2014;346 :1320-1331.Abstract

To better determine the history of modern birds, we performed a genome-scale phylogenetic analysis of 48 species representing all orders of Neoaves using phylogenomic methods created to handle genome-scale data. We recovered a highly resolved tree that confirms previously controversial sister or close relationships. We identified the first divergence in Neoaves, two groups we named Passerea and Columbea, representing independent lineages of diverse and convergently evolved land and water bird species. Among Passerea, we infer the common ancestor of core landbirds to have been an apex predator and confirm independent gains of vocal learning. Among Columbea, we identify pigeons and flamingoes as belonging to sister clades. Even with whole genomes, some of the earliest branches in Neoaves proved challenging to resolve, which was best explained by massive protein-coding sequence convergence and high levels of incomplete lineage sorting that occurred during a rapid radiation after the Cretaceous-Paleogene mass extinction event about 66 million years ago.

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2013
Dennehy JJ, Duffy S, O’Keefe KJ, Edwards SV, Turner PE. Frequent Coinfection Reduces RNA Virus Population Genetic Diversity. Journal of Heredity. 2013;104 :704-712.Abstract
The masking of deleterious mutations by complementation and the reassortment of virus segments (virus sex) are expected
to increase population genetic diversity among coinfecting viruses. Conversely, clonally reproducing or noncoinfecting virus
populations may experience clonal interference where viral clones compete with one another, preventing selective sweeps.
This dynamic reduces the efficiency of selection and increases the genetic diversity. To determine the relative influences of
these forces on population genetic diversity, we evolved 6 populations of bacteriophage φ6 under conditions promoting
or preventing coinfection. Following 300 generations, we isolated and partially sequenced 10 clones from each population.
We found greater diversity among asexual populations than sexual populations. Moreover, sexual populations did not show greater relative fitnesses than asexual populations, implying that reduced genetic variation did not result from purifying selection. However, sexual populations were less genetically robust than asexual populations and likely more prone to the deleterious epistatic effects of mutations. As such, a neutral mutation on the asexually evolved (robust) background could be profoundly deleterious on the sexually evolved (brittle) background. This could facilitate sexual populations undergoing greater purifying selection to remove deleterious mutations, but this selection is not reflected by increases in average population fitness. Our results bolster a growing literature suggesting that RNA virus segmentation is probably not a mechanism that evolved because it provides a generalized benefit of sex.
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Kultz D, Clayton DF, Robinson GE, Albertson C, Carey HV, Cummings ME, Dewar K, Edwards SV, Hofmann HA, Gross LJ, et al. New Frontiers for Organismal Biology. Bioscience. 2013;63 :464-471.Abstract

Understanding how complex organisms function as integrated units that constantly interact with their environment is a long-standing challenge in biology. To address this challenge, organismal biology reveals general organizing principles of physiological systems and behavior-in particular, in complex multicellular animals. Organismal biology also focuses on the role of individual variability in the evolutionary maintenance of diversity. To broadly advance these frontiers, cross-compatibility of experimental designs, methodological approaches, and data interpretation pipelines represents a key prerequisite. It is now possible to rapidly and systematically analyze complete genomes to elucidate genetic variation associated with traits and conditions that define individuals, populations, and species. However, genetic variation alone does not explain the varied individual physiology and behavior of complex organisms. We propose that such emergent properties of complex organisms can best be explained through a renewed emphasis on the context and life-history dependence of individual phenotypes to complement genetic data.

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Edwards SV. Next-generation QTL mapping: crowdsourcing SNPs, without pedigrees. Molecular Ecology. 2013;22 :3885-3887.Abstract

For many molecular ecologists, the mantra and mission
of the field of ecological genomics could be encapsulated
by the phrase ‘to find the genes that matter’ (Mitchell-
Olds 2001; Rockman 2012). This phrase of course refers to
the early hope and current increasing success in the
search for genes whose variation underlies phenotypic
variation and fitness in natural populations. In the years
since the modern incarnation of the field of ecological
genomics, many would agree that the low-hanging fruit
has, at least in principle, been plucked: we now have several
elegant examples of genes whose variation influences
key adaptive traits in natural populations, and these
examples have revealed important insights into the architecture
of adaptive variation (Hoekstra et al. 2006; Shapiro
et al. 2009; Chan et al. 2010). But how well will these
early examples, often involving single genes of large
effect on discrete or near-discrete phenotypes, represent
the dynamics of adaptive change for the totality of
phenotypes in nature? Will traits exhibiting continuous
rather than discrete variation in natural populations have
as simple a genetic basis as these early examples suggest
(Prasad et al. 2012; Rockman 2012)? Two papers in this
issue (Robinson et al. 2013; Santure et al. 2013) not only
suggest answers to these questions but also provide
useful extensions of statistical approaches for ecological
geneticists to study the genetics of continuous variation
in nature. Together these papers, by the same research
groups studying evolution in a natural population of
Great Tits (Parus major), provide a glimpse of what we
should expect as the field begins to dissect the genetic
basis of what is arguably the most common type of
variation in nature, and how genome-wide surveys of
variation can be applied to natural populations without
pedigrees.

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Wu S, Song S, Liu L, Edwards SV. Reply to Gatesy and Springer: the multispecies coalescent model can effectively handle recombination and gene tree heterogeneity. Proceedings of the National Academy of Sciences of the United States of America. 2013;110 :E1180. PDF
Ezaz T, Azad B, O'Meally D, Young MJ, Matsubara K, Edwards MJ, Zhang X, Holleley CE, Deakin JE, Marshall Graves JA, et al. Sequence and gene content of a large fragment of a lizard sex chromosome and evaluation of candidate sex differentiating gene R-spondin 1. Bmc Genomics. 2013;14 :899-899.Abstract

BACKGROUND: Scant genomic information from non-avian reptile sex chromosomes is available, and for only a few lizards, several snakes and one turtle species, and it represents only a small fraction of the total sex chromosome sequences in these species. RESULTS: We report a 352 kb of contiguous sequence from the sex chromosome of a squamate reptile, Pogona vitticeps, with a ZZ/ZW sex microchromosome system. This contig contains five protein coding genes (oprd1, rcc1, znf91, znf131, znf180), and major families of repetitive sequences with a high number of copies of LTR and non-LTR retrotransposons, including the CR1 and Bov-B LINEs. The two genes, oprd1 and rcc1 are part of a homologous syntenic block, which is conserved among amniotes. While oprd1 and rcc1 have no known function in sex determination or differentiation in amniotes, this homologous syntenic block in mammals and chicken also contains R-spondin 1 (rspo1), the ovarian differentiating gene in mammals. In order to explore the probability that rspo1 is sex determining in dragon lizards, genomic BAC and cDNA clones were mapped using fluorescence in situ hybridisation. Their location on an autosomal microchromosome pair, not on the ZW sex microchromosomes, eliminates rspo1 as a candidate sex determining gene in P. vitticeps. CONCLUSION: Our study has characterized the largest contiguous stretch of physically mapped sex chromosome sequence (352 kb) from a ZZ/ZW lizard species. Although this region represents only a small fraction of the sex chromosomes of P. vitticeps, it has revealed several features typically associated with sex chromosomes including the accumulation of large blocks of repetitive sequences.

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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. 2013.Abstract

Across amniotes, sex-determining mechanisms exhibit great variation, yet the genes that govern sexual differentiation are largely conserved. Studies of evolution of sex-determining and sex-differentiating genes require an exhaustive characterization of functions of those genes such as FOXL2 and FGF9. FOXL2 is associated with ovarian development, and FGF9 is known to play a role in testicular organogenesis in mammals and other amniotes. As a step toward characterization of the evolutionary history of sexual development, we measured expression of FOXL2 and FGF9 across 3 developmental stages and 8 juvenile tissue types in male and female American alligators, Alligator mississippiensis. We report surprisingly high expression of FOXL2 before the stage of embryonic development when sex is determined in response to temperature, and sustained and variable expression of FGF9 in juvenile male, but not female tissue types. Novel characterization of gene expression in reptiles with temperature-dependent sex determination such as American alligators may inform the evolution of sex-determining and sex-differentiating gene networks, as they suggest alternative functions from which the genes may have been exapted. Future functional profiling of sex-differentiating genes should similarly follow other genes and other species to enable a broad comparison across sex-determining mechanisms.

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