Publications

corrigendum to "developmental exposure to bisphenol a (bpa) alters sexual differentiation in painted turtles (chrysemys picta)" [gen. comp. endocr. 216 (2015) 77-85].		2017	28454885
medip-seq and ncpg analyses illuminate sexually dimorphic methylation of gonadal development genes with high historic methylation in turtle hatchlings with temperature-dependent sex determination.	dna methylation alters gene expression but not dna sequence and mediates some cases of phenotypic plasticity. temperature-dependent sex determination (tsd) epitomizes phenotypic plasticity where environmental temperature drives embryonic sexual fate, as occurs commonly in turtles. importantly, the temperature-specific transcription of two genes underlying gonadal differentiation is known to be induced by differential methylation in tsd fish, turtle and alligator. yet, how extensive is the link b ...	2017	28533820
corrigendum to "effects of developmental exposure to bisphenol a and ethinyl estradiol on spatial navigational learning and memory in painted turtles (chrysemys picta)" [horm. behav. 85 (2016) 48-55].		2017	28551168
annual differences in female reproductive success affect spatial and cohort-specific genotypic heterogeneity in painted turtles.	long-term ecological data were used to evaluate the relative importance of movements, breeding structure, and reproductive ecological factors to the degree of spatial and age-specific variation in genetic characteristics of painted turtles (chrysemys picta) on the e. s. george reserve in southeastern michigan. estimates of the degree of spatial genetic structuring were based on the proportion of total genotypic variance partitioned within and between subpopulations (inferred from hierarchical f- ...	1993	28564898
among-family variation for environmental sex determination in reptiles.	unlike birds and mammals, in many reptiles the temperature experienced by a developing embryo determines its gonadal sex. to understand how temperature-dependent sex determination (tsd) evolves, we must first determine the nature of genetic variation for sex ratio. here, we analyze among-family variation for sex ratio in three tsd species: the american alligator (alligator mississipiensis), the common snapping turtle (chelydra serpentina) and the painted turtle (chrysemys picta). significant fam ...	1998	28565384
morbidity and mortality of wild turtles at a north carolina wildlife clinic: a 10-year retrospective.	the medical records from 1,847 wild turtle patients seen between 2005 and 2014 by the turtle rescue team at the north carolina state university college of veterinary medicine were analyzed. eastern box turtles (terrapene carolina carolina; n = 947), yellow-bellied sliders (trachemys scripta scripta; n = 301), cooters ( pseudemys spp.; n = 235), common snapping turtles (chelydra serpentina; n = 165), and eastern painted turtles (chrysemys picta; n = 93) made up 94.3% of all patients. patient admi ...	2017	28920820
the effects of ph and pi on tension and ca2+ sensitivity of ventricular myofilaments from the anoxia-tolerant painted turtle.	we aimed to determine how increases in intracellular h+ and inorganic phosphate (pi) to levels observed during anoxic submergence affect contractility in ventricular muscle of the anoxia-tolerant western painted turtle, chrysemys picta bellii skinned multicellular preparations were exposed to six treatments with physiologically relevant levels of ph (7.4, 7.0, 6.6) and pi (3 and 8 mmol l-1). each preparation was tested in a range of calcium concentrations (pca 9.0-4.5) to determine the pca-tensi ...	2017	28939564
effects of augmented corticosterone in painted turtle eggs on offspring development and behavior.	maternal stressors can play an integral role in offspring development and ultimate behaviors in many vertebrates. increased circulating stress avoidance hormones can be reflected in elevated concentrations in ova, thus providing a potential mechanism for maternal stress to be transmitted to offspring even in taxa without parental care. in this study, we assessed the potential impacts of augmented stress avoidance hormones on offspring development and anti-predator behaviors in a freshwater turtl ...	2018	29031544
the hypoxia-tolerant vertebrate brain: arresting synaptic activity.	the ion channel arrest hypothesis has been the foundation of three decades of research into the underlying mechanisms of hypoxia/anoxia tolerance in several key species, including: painted turtles, goldfish, crucian carp, naked mole rats, and arctic and ground squirrels. the hypothesis originally stated that hypoxia/anoxia tolerant species ought to have fewer ion channels per area membrane and/or mechanisms to regulate the conductance of ion channels. today we can add to this and include mechani ...	2017	29223874
the effect of hormone manipulations on sex ratios varies with environmental conditions in a turtle with temperature-dependent sex determination.	exogenous application of steroids and related substances to eggs affects offspring sex ratios in species with temperature-dependent sex determination (tsd). laboratory studies demonstrate that this effect is most pronounced near the constant temperature that produces 1:1 sex ratios (i.e., pivotal temperature). however, the impact of such chemicals on sex determination under natural nest temperatures (which fluctuate daily) is unknown, but could provide insight into the relative contributions of ...	2017	29356364
a new slider turtle (testudines: emydidae: deirochelyinae:trachemys) from the late hemphillian (late miocene/early pliocene) of eastern tennessee and the evolution of the deirochelyines.	trachemys(testudines: emydidae) represents one of the most well-known turtle genera today. the evolution oftrachemys, while being heavily documented with fossil representatives, is not well understood. numerous fossils from the late hemphillian gray fossil site (gfs) in northeastern tennessee help to elucidate its evolution. the fossiltrachemysat the gfs represent a new species. the new taxon,trachemys haugrudi, is described, and currently represents the most thoroughly described fossil emydid s ...	2018	29456887
effects of urbanization on the population structure of freshwater turtles across the united states.	landscape-scale alterations that accompany urbanization may negatively affect the population structure of wildlife species such as freshwater turtles. changes to nesting sites and higher mortality rates due to vehicular collisions and increased predator populations may particularly affect immature turtles and mature female turtles. we hypothesized that the proportions of adult female and immature turtles in a population will negatively correlate with landscape urbanization. as a collaborative ef ...	2018	29781169
seasonal variations in oviductal morphology of the painted turtle, chrysemys picta.	histology of each of the five segments of the oviduct of the female turtle chrysemys picta was described for successive intervals throughout their annual cycle. uterine and glandular segments showed marked seasonal variations in the extent and content of the submucosal and epithelial glands. submucosal glands were most prominent in preovulatory and postovulatory animals (may to june), regressing in late summer (oviposited animals) and recrudescing the following spring. these changes correlated w ...	1991	29865522
the development and homology of the chelonian carpus and tarsus.	the long-standing controversies involving the number and homologies of the elements of the carpus and tarsus of turtles are reviewed from a developmental perspective. the analysis is based on a detailed description of the chondrogenesis of the carpus and tarsus in the species chelydra serpentina and chrysemys picta. the first stage described is the differentiation of a y-shaped chondrogenetic condensation involving the humerus (femur)-radius/ ulna (tibia/fibula). this stage is followed by the ea ...	1985	30005563
small non-coding rna expression and vertebrate anoxia tolerance.	background: extreme anoxia tolerance requires a metabolic depression whose modulation could involve small non-coding rnas (small ncrnas), which are specific, rapid, and reversible regulators of gene expression. a previous study of small ncrna expression in embryos of the annual killifish austrofundulus limnaeus, the most anoxia-tolerant vertebrate known, revealed a specific expression pattern of small ncrnas that could play important roles in anoxia tolerance. here, we conduct a comparative stud ...	2018	30042786
changes in the material properties of the shell during simulated aquatic hibernation in the anoxia-tolerant painted turtle.	western painted turtles (chrysemys picta bellii) tolerate anoxic submergence longer than any other tetrapod, surviving more than 170 days at 3°c. this ability is due, in part, to the shell and skeleton simultaneously releasing calcium and magnesium carbonates, and sequestering lactate and h+ to prevent lethal decreases in body fluid ph. we evaluated the effects of anoxic submergence at 3°c on various material properties of painted turtle bone after 60, 130 and 167-170 days, and compared them wit ...	2018	30065038
colonization and usage of an artificial urban wetland complex by freshwater turtles.	conservation authorities invest heavily in the restoration and/or creation of wetlands to counteract the destruction of habitat caused by urbanization. monitoring the colonization of these new wetlands is critical to an adaptive management process. we conducted a turtle mark-recapture survey in a 250 ha artificially created wetland complex in a large north american city (toronto, ontario). we found that two of ontario's eight native turtle species (snapping turtle (sn), chelydra serpentina, and ...	2018	30123718
disentangling the genetic effects of refugial isolation and range expansion in a trans-continentally distributed species.	in wide-ranging taxa with historically dynamic ranges, past allopatric isolation and range expansion can both influence the current structure of genetic diversity. considering alternate historical scenarios involving expansion from either a single refugium or from multiple refugia can be useful in differentiating the effects of isolation and expansion. here, we examined patterns of genetic variability in the trans-continentally distributed painted turtle (chrysemys picta). we utilized an existin ...	2019	30171190
the role of acetylcholine in attention in turtles (chrysemys picta).	research on mammals and turtles has suggested that acetylcholine is involved in attention in these groups. two experiments investigated the ability of painted turtles (chrysemys picta) to ignore irrelevant stimuli when the basal forebrain acetylcholine system was compromised. in experiment 1, turtles given lesions of the basal magnocellular cholinergic nucleus (nbm) or sham lesions were tested on a go/no go discrimination between horizontal and vertical stripes with or without irrelevant inserts ...	2018	30176658
environmentally induced phenotypic plasticity explains hatching synchrony in the freshwater turtle chrysemys picta.	environmentally cued hatching allows embryos to alter the time of hatching in relation to environment through phenotypic plasticity. spatially variable temperatures within shallow nests of many freshwater turtles cause asynchronous development of embryos within clutches, yet neonates still hatch synchronously either by hatching early or via metabolic compensation. metabolic compensation and changes in circadian rhythms presumably enable embryos to adjust their developmental rates to catch up to ...	2018	30192440
taurine activates glycine and gabaa receptor currents in anoxia-tolerant painted turtle pyramidal neurons.	unlike anoxia-intolerant mammals, painted turtles can survive extended periods without oxygen. this is partly accomplished by an anoxia-mediated increase in gamma-aminobutyric acid (gaba) release, which activates gaba receptors and mediates spike arrest in turtle neurons via shunting inhibition. extracellular taurine levels also increase during anoxia; why this occurs is unknown but it is speculated that glycine and/or gabaa/b receptors are involved. given the general importance of inhibitory ne ...	2018	30237241
ultrastructure of the parathyroid gland of fresh-water turtles.	the parathyroid glands of fresh-water turtles (pseudemys scripta and chrysemys picta) are composed of cords of cells in which dark and light variants of chief cells and occasional oxyphil cells can be distinguished. cytoplasmic granules measuring about 0.3-0.4 μm and all the cellular organelles associated with protein and carbohydrate synthesis can be seen in both dark and light chief cells; the cytoplasm of oxyphils is packed with mitochondria which obscure other organelles. an unusual feature ...	1972	30366482
evolutionary conservation of transferrin genomic organization and expression characterization in seven freshwater turtles.	serum transferrin (tf), encoding an iron-binding glycoprotein, has been revealed to play important roles in iron transportation and immune response, and it also has been demonstrated to be valuable for phylogenetic analysis in vertebrates. however, the evolutionary conservation, expression profiles and positive selection of transferrin genes among freshwater turtle species remain largely unclear. here, the genomic dna and coding sequences of transferrin genes were cloned and characterized in sev ...	2018	30392910
of molecules, memories and migration: m1 acetylcholine receptors facilitate spatial memory formation and recall during migratory navigation.	many animals use complex cognitive processes, including the formation and recall of memories, for successful navigation. however, the developmental and neurological processes underlying these cognitive aspects of navigation are poorly understood. to address the importance of the formation and recollection of memories during navigation, we pharmacologically manipulated turtles (chrysemys picta) that navigate long distances using precise, complex paths learned during a juvenile critical period. we ...	2018	30429306
the effect of dietary carotenoid increase on painted turtle spot and stripe color.	determination of how carotenoid-based color patches change with pigmentary access is important to understanding color patch function in animals. we performed a carotenoid addition experiment on male painted turtles (chrysemys picta) to determine if an increase in dietary carotenoids led to location-specific changes in painted turtle spot and stripe color. turtles fed large quantities of carotenoids had increased yellow chroma in chin stripes and increased red chroma in the neck and carapace stri ...	2019	30557612
detecting coevolution of positively selected in turtles sperm-egg fusion proteins.	physically interacting sperm-egg proteins have been identified using gene-modified animals in some mammal species. three proteins are essential for sperm-egg binding: izumo1 on the sperm surface, and juno and cd9 on the egg surface. most proteins linked to reproductive function evolve rapidly among species by positive selection, and have correlated evolutionary rates to compensate for changes on both the sperm and egg. up to now, interactions between sperm and egg proteins have not been identifi ...	2019	30790628
extreme thermal fluctuations from climate change unexpectedly accelerate demographic collapse of vertebrates with temperature-dependent sex determination.	global climate is warming rapidly, threatening vertebrates with temperature-dependent sex determination (tsd) by disrupting sex ratios and other traits. less understood are the effects of increased thermal fluctuations predicted to accompany climate change. greater fluctuations could accelerate feminization of species that produce females under warmer conditions (further endangering tsd animals), or counter it (reducing extinction risk). here we use novel experiments exposing eggs of painted tur ...	2019	30862793
geographic variation in thermal sensitivity of early life traits in a widespread reptile.	taxa with large geographic distributions generally encompass diverse macroclimatic conditions, potentially requiring local adaptation and/or phenotypic plasticity to match their phenotypes to differing environments. these eco-evolutionary processes are of particular interest in organisms with traits that are directly affected by temperature, such as embryonic development in oviparous ectotherms. here we examine the spatial distribution of fitness-related early life phenotypes across the range of ...	2019	30891217
heterogeneous bioapatite carbonation in western painted turtles is unchanged after anoxia.	adsorbed and structurally incorporated carbonate in bioapatite, the primary mineral phase of bone, is observed across vertebrates, typically at 2-8 wt%, and supports critical physiological and biochemical functions. several turtle species contain elevated bone-associated carbonate, a property linked to ph buffering and overwintering survival. prior studies of turtle bone utilized bulk analyses, which do not provide spatial resolution of carbonate. using raman spectroscopy, the goals of this stud ...	2019	30930203
mitochondrial matrix ph acidifies during anoxia and is maintained by the f1fo-atpase in anoxia-tolerant painted turtle cortical neurons.	the western painted turtle (chrysemys picta bellii) can survive extended periods of anoxia via a series of mechanisms that serve to reduce its energetic needs. central to these mechanisms is the response of mitochondria, which depolarize in response to anoxia in turtle pyramidal neurons due to an influx of k+. it is currently unknown how mitochondrial matrix ph is affected by this response and we hypothesized that matrix ph acidifies during anoxia due to increased k+/h+ exchanger activity. inhib ...	2019	30984533
oxygen-sensitive interneurons exhibit increased activity and gaba release during ros scavenging in the cerebral cortex of the western painted turtle.	the western painted turtle (chrysemys picta bellii) has the unique ability of surviving several months in the absence of oxygen, which is termed anoxia. one major protective strategy that the turtle employs during anoxia is a reduction in neuronal electrical activity, which may result from a natural reduction in reactive oxygen species (ros). we previously linked a reduction in ros levels to an increase in γ-amino butyric acid (gaba) receptor currents. the purpose of this study is to understand ...	2019	31141433
joint estimation of growth and survival from mark-recapture data to improve estimates of senescence in wild populations.	understanding age-dependent patterns of survival is fundamental to predicting population dynamics, understanding selective pressures, and estimating rates of senescence. however, quantifying age-specific survival in wild populations poses significant logistical and statistical challenges. recent work has helped to alleviate these constraints by demonstrating that age-specific survival can be estimated using mark-recapture data even when age is unknown for all or some individuals. however, previo ...	2020	31471965
detecting trends in body size: empirical and statistical requirements for intraspecific analyses.	attributing biological explanations to observed ecogeographical and ecological patterns require eliminating potential statistical and sampling artifacts as alternative explanations of the observed patterns. here, we assess the role of sample size, statistical power, and geographic inclusivity on the general validity and statistical significance of relationships between body size and latitude for 3 well-studied species of turtles. we extend those analyses to emphasize the importance of using stat ...	2019	31616479
analysis of the microbiota in the fecal material of painted turtles (chrysemys picta).	we used high-throughput sequencing analysis, which targeted the hypervariable v3-v4 region of the bacterial 16s rrna gene, to investigate the microbiota in fecal material from ten wild painted turtles (chrysemys picta) captured in southeastern wisconsin. the most predominant bacterial phylum detected in all samples was the firmicutes (relative abundance for all samples 96.4% to 68.3%). the next most predominant phylum was bacteroidetes (relative abundance for all samples 23.9% to 7.8%) in eight ...	2020	31642965
navigating oxygen deprivation: liver transcriptomic responses of the red eared slider turtle to environmental anoxia.	the best facultative anaerobes among vertebrates are members of the genera trachemys (pond slider turtles) and chrysemys (painted turtles), and are able to survive without oxygen for up to 12 to 18 weeks at ∼3 °c. in this study, we utilized rnaseq to profile the transcriptomic changes that take place in response to 20 hrs of anoxia at 5 °c in the liver of the red eared slide turtle (trachemys scripta elegans). sequencing reads were obtained from at least 18,169 different genes and represented a ...	2019	31788367
sex and incubation temperature independently affect embryonic development and offspring size in a turtle with temperature-dependent sex determination.	developmental environments can have lasting effects on an individual's phenotype. in many reptiles, for example, egg incubation temperature permanently determines offspring sex (temperature-dependent sex determination, tsd) and also influences a suite of morphological, physiological, and behavioral traits. thus, the contributions of sex and incubation temperature to phenotypic variation are difficult to identify because these factors are confounded under tsd. we used chemical manipulations to ex ...	2020	31808735
development-specific transcriptomic profiling suggests new mechanisms for anoxic survival in the ventricle of overwintering turtles.	oxygen deprivation swiftly damages tissues in most animals, yet some species show remarkable abilities to tolerate little or even no oxygen. painted turtles exhibit a development-dependent tolerance that allows adults to survive anoxia approximately four times longer than hatchlings: adults survive ∼170 days and hatchlings survive ∼40 days at 3°c. we hypothesized that this difference is related to development-dependent differences in ventricular gene expression. using a comparative ontogenetic a ...	2020	31862849
composition and divergence of coronavirus spike proteins and host ace2 receptors predict potential intermediate hosts of sars-cov-2.	from the beginning of 2002 and 2012, severe respiratory syndrome coronavirus (sars-cov) and middle east respiratory syndrome coronavirus (mers-cov) crossed the species barriers to infect humans, causing thousands of infections and hundreds of deaths, respectively. currently, a novel coronavirus (sars-cov-2), which has become the cause of the outbreak of coronavirus disease 2019 (covid-19), was discovered. until 18 february 2020, there were 72 533 confirmed covid-19 cases (including 10 644 severe ...	2020	32100877
high prevalence of subclinical frog virus 3 infection in freshwater turtles of ontario, canada.	ranaviruses have been associated with chelonian mortality. in canada, the first two cases of ranavirus were detected in turtles in 2018 in ontario, although a subsequent survey of its prevalence failed to detect additional positive cases. to confirm the prevalence of ranavirus in turtles in ontario, we used a more sensitive method to investigate if lower level persistent infection was present in the population. here we report results via a combination of qpcr, pcr, sanger sequencing and genome s ...	2020	32174301
alternative splicing and thermosensitive expression of dmrt1 during urogenital development in the painted turtle, chrysemys picta.	the doublesex and mab-3 related transcription factor 1 (dmrt1) is a highly conserved gene across numerous vertebrates and invertebrates in sequence and function. small aminoacid changes in dmrt1 are associated with turnovers in sex determination in reptiles. dmrt1 is upregulated in males during gonadal development in many species, including the painted turtle, chrysemys picta, a reptile with temperature-dependent sex determination (tsd). dmrt1 is reported to play different roles during sex deter ...	2020	32219017
immunosenescence and its influence on reproduction in a long-lived vertebrate.	immunosenescence is a well-known phenomenon in mammal systems, but its relevance in other long-lived vertebrates is less understood. further, the influence of age and reproductive effort on immune function in long-lived species can be challenging to assess, as long-term data are scarce and it is often difficult to sample the oldest age classes. we used the painted turtle (chrysemys picta) to test hypotheses of immunosenescence and a trade-off between reproductive output and immune function in a ...	2020	32376708
karyotypic evolution of sauropsid vertebrates illuminated by optical and physical mapping of the painted turtle and slider turtle genomes.	recent sequencing and software enhancements have advanced our understanding of the evolution of genomic structure and function, especially addressing novel evolutionary biology questions. yet fragmentary turtle genome assemblies remain a challenge to fully decipher the genetic architecture of adaptive evolution. here, we use optical mapping to improve the contiguity of the painted turtle (chrysemys picta) genome assembly and use de novo fluorescent in situ hybridization (fish) of bacterial artif ...	2020	32806747
becoming creatures of habit: among- and within-individual variation in nesting behaviour shift with age.	the quantification of repeatability has enabled behavioural and evolutionary ecologists to assess the heritable potential of traits. for behavioural traits that vary across life, age-related variation should be accounted for to prevent biasing the microevolutionary estimate of interest. moreover, to gain a mechanistic understanding of ontogenetic variation in behaviour, among- and within-individual variance should be quantified across life. we leveraged a 30-year study of painted turtles (chryse ...	2020	32897610
sex-specific growth, shape, and their impacts on the life history of a long-lived vertebrate.	individual growth rates both comprise and determine life-history phenotypes. despite decades of interest in understanding the relationship between individual growth and life history, chelonian longevity has limited our ability to robustly estimate individual growth curves that span the life of both sexes.	2018	32944008
evaluation of a multiplexed, multispecies nuclear receptor assay for chemical hazard assessment.	sensitivity to potential endocrine disrupting chemicals in the environment varies across species and is influenced by sequence conservation of their nuclear receptor targets. here, we evaluated a multiplexed, in vitro assay testing receptors relevant to endocrine and metabolic disruption from five species. the trans-factorial™ system of human nuclear receptors was modified to include additional species: mouse (mus musculus), frog (xenopus laevis), zebrafish (danio rerio), chicken (gallus gallus) ...	2020	33049310