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During embryonic development, organisms are sensitive to changes in thyroid hormone signaling which can reset the hypothalamic-pituitary-thyroid axis. It has been hypothesized that this developmental programming is a 'predictive adaptive response', a physiological adjustment in accordance with the embryonic environment that will best aid an individ...
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... Increased salinity also appears to influence thyroid development and thyroid hormone (TH) secretion in alligators, which unlike many species of crocodiles, do not have extrarenal salt glands. Neonatal American alligators hatched from eggs collected from an estuarine barrier island population exhibited thyroid hyperplasia and higher triiodothyronine (T 3 ) concentrations than neonates from an inland population (Boggs et al., 2013). Although these differences do not persist in hatchlings maintained in freshwater conditions, juvenile alligators from the barrier island population have higher TH concentrations and lower plasma inorganic iodide (pI À ) in comparison to the inland population (Boggs et al., 2011). ...
... A further well-known case of endocrine disruption in a wild population is the American alligators, Alligator mississippiensis, inhabiting the polluted Lake Apopka, Florida, United States, where both males and female alligators were shown to exhibit developmental abnormalities in their reproductive systems (Guillette et al., 1994;Guillette et al., 1996). Moreover, the thyroid systems of juvenile Lake Apopka alligators were also significantly impacted with abnormal thyroid anatomy and thyroid hormone levels being observed in hatchlings (Boggs et al., 2013;Crain et al., 1998) The potential sources of EDCs in the CRC include WWTW, agriculture (crops, livestock, aquaculture), forestry, landfills, paper and pulp effluent, trace metals and mining and metallurgy. ...
... While no relevant studies were reported in birds, in a study investigating the impact of embryonic sex steroid exposure on thyroid physiology in the American alligator (Alligator mississippiensis) from the EDCcontaminated Lake Apopka, results suggested that estradiol exposure did not impact thyroid physiology in these alligators (Galligan et al., 2019). This indicated that the effect of in ovo organochlorine pesticide exposure on the organization of the thyroid reported in a related study on this species (Boggs et al., 2013) was not mediated through estrogens. ...
... Analyses from Lake Apopka alligators demonstrated that embryonic androgen (dihydrotestosterone) exposure did not impact thyroid physiology (Galligan et al., 2019). This indicated that the effect of in ovo organochlorine pesticide exposure on the organization of the thyroid reported in a related study on this species (Boggs et al., 2013) was not mediated through steroid hormones. The authors could therefore not conclude that thyroidal physiology in the American alligator is sensitive to steroid hormone signaling at early life stages. ...
Thyroid hormones (THs) are important regulators of growth, development, and homeostasis of all vertebrates. There are many environmental contaminants that are known to disrupt TH action, yet their mechanisms are only partially understood. While the effects of Endocrine Disrupting Chemicals (EDCs) are mostly studied as “hormone system silos”, the present critical review highlights the complexity of EDCs interfering with TH function through their interactions with other hormonal axes involved in reproduction, stress, and energy metabolism. The impact of EDCs on components that are shared between hormone signaling pathways or intersect between pathways can thus extend beyond the molecular ramifications to cellular, physiological, behavioral, and whole-body consequences for exposed organisms. The comparatively more extensive studies conducted in mammalian models provides encouraging support for expanded investigation and highlight the paucity of data generated in other non-mammalian vertebrate classes. As greater genomics-based resources become available across vertebrate classes, better identification and delineation of EDC effects, modes of action, and identification of effective biomarkers suitable for HPT disruption is possible. EDC-derived effects are likely to cascade into a plurality of physiological effects far more complex than the few variables tested within any research studies. The field should move towards understanding a system of hormonal systems’ interactions rather than maintaining hormone system silos.
... Given that snapping turtles were studied a few days after hatching, longer-term studies will be required to distinguish whether these effects are simply due to thermal acclimation or are the result of developmental programming of metabolic phenotype. Nevertheless, studies of American alligators do suggest that disruption of thyroid hormone signaling during embryogenesis can program functioning of the hypothalamic-pituitary-thyroid axis as long as 10 months after hatching (Boggs et al., 2013). ...
Reptiles are critically affected by temperature throughout their lifespan, but especially so during early development. Temperature-induced changes in phenotype are a specific example of a broader phenomenon called phenotypic plasticity in which a single individual is able to develop different phenotypes when exposed to different environments. With climate change occurring at an unprecedented rate, it is important to study temperature effects on reptiles. For example, the potential impact of global warming is especially pronounced in species with temperature-dependent sex determination (TSD) because temperature has a direct effect on a key phenotypic (sex) and demographic (population sex ratios) trait. Reptiles with TSD also serve as models for studying temperature effects on the development of other traits that display continuous variation. Temperature directly influences metabolic and developmental rate of embryos and can have permanent effects on phenotype that last beyond the embryonic period. For instance, incubation temperature programs post-hatching hormone production and growth physiology, which can profoundly influence fitness. Here, we review current knowledge of temperature effects on phenotypic and developmental plasticity in reptiles. First, we examine the direct effect of temperature on biophysical processes, the concept of thermal performance curves, and the process of thermal acclimation. After discussing these reversible temperature effects, we focus the bulk of the review on developmental programming of phenotype by temperature during embryogenesis (i.e., permanent developmental effects). We focus on oviparous species because eggs are especially susceptible to changes in ambient temperature. We then discuss recent work probing the role of epigenetic mechanisms in mediating temperature effects on phenotype. Based on phenotypic effects of temperature, we return to the potential impact of global warming on reptiles. Finally, we highlight key areas for future research, including the identification of temperature sensors and assessment of genetic variation for thermosensitivity.
... American alligators (Alligator mississippiensis) inhabiting Lake Apopka (Orange county, Florida, USA), a site contaminated with OCPs (Guillette Jr. et al., 1999;Heinz et al., 1991), exhibit altered thyroidal phenotypes that include diminished neonatal plasma TH concentrations, altered thyroidal histomorphology, and impaired growth (Boggs et al., 2013), as well as disrupted reproductive physiology, including gonadal transcription, steroidogenesis, and systemic steroid hormone homeostasis (Crain et al., 1998;Guillette et al., 1994Guillette et al., , 1995Guillette et al., , 1996Guillette et al., , 1999Moore et al., 2012). Importantly, these effects are persistent; Boggs et al. (2013) and Moore et al. (2012) demonstrated that these impaired thyroidal and gonadal phenotypes, respectively, remain present in Lake Apopka animals raised under controlled laboratory conditions for months, indicating that in ovo OCP exposure induces organizational effects with long-lasting consequences on the alligator endocrine system. ...
... American alligators (Alligator mississippiensis) inhabiting Lake Apopka (Orange county, Florida, USA), a site contaminated with OCPs (Guillette Jr. et al., 1999;Heinz et al., 1991), exhibit altered thyroidal phenotypes that include diminished neonatal plasma TH concentrations, altered thyroidal histomorphology, and impaired growth (Boggs et al., 2013), as well as disrupted reproductive physiology, including gonadal transcription, steroidogenesis, and systemic steroid hormone homeostasis (Crain et al., 1998;Guillette et al., 1994Guillette et al., , 1995Guillette et al., , 1996Guillette et al., , 1999Moore et al., 2012). Importantly, these effects are persistent; Boggs et al. (2013) and Moore et al. (2012) demonstrated that these impaired thyroidal and gonadal phenotypes, respectively, remain present in Lake Apopka animals raised under controlled laboratory conditions for months, indicating that in ovo OCP exposure induces organizational effects with long-lasting consequences on the alligator endocrine system. Thus, the Lake Apopka alligator population presents a unique opportunity to examine the effects of steroid hormone disruption on both short-and long-term thyroid physiology under realistic exposure conditions. ...
... Using an ecologically relevant model in which persistent thyroidal abnormalities have been linked to OCP exposure, we describe both the native transcriptional patterns of genes related to thyroid function and steroid hormone signaling in the alligator embryo, as well as the functional consequences of embryonic exposure to exogenous steroid hormones on transcription of these genes later in life. While embryonic stages are critical windows of thyroid hormone activity in vertebrates, previous studies of American alligator thyroidal physiology have not described embryonic life stages (Bermudez et al., 2011;Boggs et al., 2013Boggs et al., , 2016. In this study we test two competing hypotheses regarding the roles that steroid hormones play in mediating OCP-induced thyroid disruption. ...
The thyroid gland is sensitive to steroid hormone signaling, and many thyroid disrupting contaminants also disrupt steroid hormone homeostasis, presenting the possibility that thyroid disruption may occur through altered steroid hormone signaling. To examine this possibility, we studied short-term and persistent impacts of embryonic sex steroid exposure on thyroid physiology in the American alligator. Alligators from a lake contaminated with endocrine disrupting contaminants (Lake Apopka, FL, USA) have been shown to display characteristics of thyroid and steroid hormone disruption. Previous studies suggest these alterations arise during development and raise the possibility that exposure to maternally deposited contaminants might underlie persistent organizational changes in both thyroidal and reproductive function. Thus, this population provides a system to investigate contaminant-mediated organizational thyroid disruption in an environmentally-relevant context. We assess the developmental expression of genetic pathways involved in thyroid hormone biosynthesis and find that expression of these genes increases prior to hatching. Further, we show that nuclear steroid hormone receptors are also expressed during this period, indicating the developing thyroid is potentially responsive to steroid hormone signaling. We then explore functional roles of steroid signaling during development on subsequent thyroid function in juvenile alligators. We exposed alligator eggs collected from both Lake Apopka and a reference site to 17β-estradiol and a non-aromatizable androgen during embryonic development, and investigated effects of exposure on hatchling morphometrics and thyroidal gene expression profiles at 5 months of age. Steroid hormone treatment did not impact the timing of hatching or hatchling size. Furthermore, treatment with steroid hormones did not result in detectable impacts on thyroid transcriptional programs, suggesting that precocious or excess estrogen and androgen exposure does not influence immediate or long-term thyroidal physiology.
... However, a critical dependence upon estrogen signals presents a vulnerability to the influence of exogenous endocrine cues, including those in the form of environmental contaminants. Deleterious effects of environmental endocrine disrupting contaminants (EDCs) have been uncovered in a broad suite of wildlife, including thyroid abnormalities [5][6][7], production of intersex individuals [8,9], decreased fertility [10][11][12][13], and general population decline [12,14,15]. These early studies pioneered our current understanding of endocrine disruption and ultimately contributed to the "developmental origins of health and disease" hypothesis [16,17]. ...
Estrogens regulate key aspects of sexual determination and differentiation, and exposure to exogenous estrogens can alter ovarian development. Alligators inhabiting Lake Apopka, FL are historically exposed to estrogenic endocrine disrupting contaminants and are characterized by a suite of reproductive abnormalities, including altered ovarian gene expression and abated transcriptional responses to follicle stimulating hormone. Here, we test the hypothesis that disrupting estrogen signaling during gonadal differentiation results in persistent alterations to ovarian gene expression that mirror alterations observed in alligators from Lake Apopka. Alligator embryos collected from a reference site lacking environmental contamination were exposed to estradiol-17 beta or a non-aromatizable androgen in ovo and raised to the juvenile stage. Changes in basal and gonadotropin-challenged ovarian gene expression were then compared to Apopka juveniles raised under identical conditions. Assessing basal transcription in untreated reference and Apopka animals revealed a consistent pattern of differential expression of key ovarian genes. For each gene where basal expression differed across sites, in ovo estradiol treatment in reference individuals recapitulated patterns observed in Apopka alligators. Among those genes affected by site and estradiol treatment were three aryl hydrocarbon receptor (AHR) isoforms, suggesting that developmental estrogen signaling might program sensitivity to AHR ligands later in life. Treatment with gonadotropins stimulated strong ovarian transcriptional responses, however, the magnitude of responses was not strongly affected by steroid hormone treatment. Collectively, these findings demonstrate that precocious estrogen signaling in the developing ovary likely underlies altered transcriptional profiles observed in a natural population exposed to endocrine disrupting contaminants.
... Beginning in 2006, the late Dr. L. J. Guillette Jr. (a summary of Dr. Guillette Jr.'s accomplishments can be found in McCoy et al. 2016) in collaboration with researchers from the Kennedy Space Center-Ecological Program and individuals from several universities, commenced a comprehensive population-scale study of alligator reproductive physiology and behavior, ecotoxicology, health, and ecology within the Merritt Island National Wildlife Refuge and greater Cape Canaveral Peninsula located along the mid-Atlantic coast of Florida (Boggs et al. 2011, Boggs et al. 2013, Bowden et al. 2014a, Bowden et al. 2014b, Horai et al. 2014, Tellez and Nifong 2014, Rosenblatt et al. 2015, Bangma et al. 2017a, Bangma et al. 2017b, Nifong and Lowers 2017. While the Cape Canaveral Peninsula is not a true barrier island, the majority of upland areas along the peninsula are surrounded by saline waters and are ecologically analogous to barrier islands. ...
... Boggs et al. (2011) hypothesized that altered iodide, a vital structural component of thyroid hormones, linked to differences in iodine content within the diet, likely contributed to the perpetually elevated thyroid hormone concentrations observed in alligators from MINWR. Boggs et al. (2013) further investigated the relationship between and the potential implications (i.e., adult metabolic diseases) of iodine exposure to thyroid functioning and morphology in developing (i.e., embryonic) alligators. Boggs et al. (2013) demonstrated that embryonic exposure to elevated iodine and other endocrine disrupting chemicals can alter the morphology and function of the thyroid gland, which could potentially lead to the development of harmful thyroid syndromes later in life (i.e., thyrotoxicosis, hyper-or hypo-thyroidism). ...
... Boggs et al. (2013) further investigated the relationship between and the potential implications (i.e., adult metabolic diseases) of iodine exposure to thyroid functioning and morphology in developing (i.e., embryonic) alligators. Boggs et al. (2013) demonstrated that embryonic exposure to elevated iodine and other endocrine disrupting chemicals can alter the morphology and function of the thyroid gland, which could potentially lead to the development of harmful thyroid syndromes later in life (i.e., thyrotoxicosis, hyper-or hypo-thyroidism). Iodine content is much higher in the tissues of estuarine-versus freshwater-and terrestrial-inhabiting prey, thus the degree to which coastal alligators consume estuarine prey could potentially influence thyroid hormone production and metabolism. ...
The conservation history of the American alligator (Alligator mississippiensis) has come full circle within the history of the United States; alligators are espoused as a successful example of American wildlife management. Alligators were awed and feared by early naturalists and settlers, who considered them abundant and widespread. Alligators were considered a nuisance and often killed for sport or when conflicts with human interests occurred. However, early conflicts were infrequent and had a negligible impact on alligator populations. Beginning in the 1850’s, products made from alligator hide became fashionable; hence, alligators were hunted commercially. The introduction of automobiles and outboard boat motors intensified alligator harvests by making previously inaccessible areas accessible to hunters, which resulted in declines of alligator populations. Draining of wetlands for agriculture and mineral exploration during the early 1900’s further reduced alligator populations, which by the 1960’s alligator populations reached their lowest numbers. In 1967 alligators were awarded protection under the Endangered Species Preservation Act of 1966, and later classified as an endangered species under the Endangered Species Act of 1973. The halt of hunting activities allowed alligator numbers to rebound. By 1987 alligators were reclassified as threatened due to ‘similarity of appearance’ with other threatened and endangered crocodilians. Market hunting and egg collection was reestablished, but is now regulated by state wildlife agencies. Due to increased urbanization of historically rural areas, human-alligator conflicts are on the rise; thus, creating a human culture where alligators are once again considered a nuisance species.
... Beginning in 2006, the late Dr. L. J. Guillette Jr. (a summary of Dr. Guillette Jr.'s accomplishments can be found in McCoy et al. 2016) in collaboration with researchers from the Kennedy Space Center-Ecological Program and individuals from several universities, commenced a comprehensive population-scale study of alligator reproductive physiology and behavior, ecotoxicology, health, and ecology within the Merritt Island National Wildlife Refuge and greater Cape Canaveral Peninsula located along the mid-Atlantic coast of Florida (Boggs et al. 2011, Boggs et al. 2013, Bowden et al. 2014a, Bowden et al. 2014b, Horai et al. 2014, Tellez and Nifong 2014, Rosenblatt et al. 2015, Bangma et al. 2017a, Bangma et al. 2017b, Nifong and Lowers 2017. While the Cape Canaveral Peninsula is not a true barrier island, the majority of upland areas along the peninsula are surrounded by saline waters and are ecologically analogous to barrier islands. ...
... Boggs et al. (2011) hypothesized that altered iodide, a vital structural component of thyroid hormones, linked to differences in iodine content within the diet, likely contributed to the perpetually elevated thyroid hormone concentrations observed in alligators from MINWR. Boggs et al. (2013) further investigated the relationship between and the potential implications (i.e., adult metabolic diseases) of iodine exposure to thyroid functioning and morphology in developing (i.e., embryonic) alligators. Boggs et al. (2013) demonstrated that embryonic exposure to elevated iodine and other endocrine disrupting chemicals can alter the morphology and function of the thyroid gland, which could potentially lead to the development of harmful thyroid syndromes later in life (i.e., thyrotoxicosis, hyper-or hypo-thyroidism). ...
... Boggs et al. (2013) further investigated the relationship between and the potential implications (i.e., adult metabolic diseases) of iodine exposure to thyroid functioning and morphology in developing (i.e., embryonic) alligators. Boggs et al. (2013) demonstrated that embryonic exposure to elevated iodine and other endocrine disrupting chemicals can alter the morphology and function of the thyroid gland, which could potentially lead to the development of harmful thyroid syndromes later in life (i.e., thyrotoxicosis, hyper-or hypo-thyroidism). Iodine content is much higher in the tissues of estuarine-versus freshwater-and terrestrial-inhabiting prey, thus the degree to which coastal alligators consume estuarine prey could potentially influence thyroid hormone production and metabolism. ...
... 28 59 0 N, long. 80 61 0 W) (Boggs et al., 2013;Burger et al., 2000;Garrison et al., 2010;Guillette et al., 1994Guillette et al., , 1999Heinz et al., 1991;Horai et al., 2014). Lake Apopka is heavily contaminated with organochlorine pesticides from an industrial spill in the 1980s (e.g. ...
Sub-individual biomarkers are sub-lethal biological responses commonly used in the assessment of wildlife exposure to environmental contaminants. In this study, we examined the activity of glutathione-s-transferase (GST) and lactate dehydrogenase (LDH), and metallothionein (MT) concentrations among captive-raised alligator hatchlings, wild-caught juveniles, and wild-caught adults. Juveniles and adults were collected from three locations in Florida (USA) with varying degrees of contamination (i.e. Lake Apopka (organochlorine polluted site), Merritt Island National Wildlife Refuge (NWR) (metal polluted site), and Lake Woodruff NWR (reference site)). We examined whether changes in the response of these three biomarkers were age and sex dependent or reflected site-specific variations of environmental contaminants. Juvenile alligators from Merritt Island NWR had higher MT concentrations and lower GST activity compared to those from the other two sites. This outcome was consistent with higher metal pollution at this location. Sexually dimorphic patterns of MT and GST (F > M) were observed in juvenile alligators from all sites, although this pattern was not observed in adults. GST activity was lower in captive-raised alligators from Lake Apopka and Merritt Island NWR as compared to animals from Lake Woodruff NWR, suggesting a possible developmental modulator at these sites. No clear patterns were observed in LDH activity. We concluded that GST and MT demonstrate age and sex specific patterns in the alligators inhabiting these study sites and that the observed variation among sites could be due to differences in contaminant exposure.
... Iodine is a dietary nutrient required for the production of the thyroid hormones thyroxine and triiodothyronine (T 4 and T 3 , respectively), which contribute to regulation of growth, metabolism, and reproduction (Flamant and Samarut, 2003;Trokoudes et al., 2006;Umpleby and Russell-Jones, 1996). A diet overly rich in iodine can induce hypothyroidism or hyperthyroidism in some species (Markou et al., 2001;Martin et al., 2000;Stanbury et al., 1998) and has been linked to hyperthyroid biomarkers in neonatal American alligators (Boggs et al., 2013). It thereby follows that because iodine is elevated in saltwater and marine prey compared to freshwater prey items and iodine is a nutrient required for production of thyroid hormones, alligators in coastal regions could have altered thyroid horhttp://dx.doi.org/10.1016/j.ygcen.2015.12.006 0016-6480/Published by Elsevier Inc. mone concentrations due to an increased exposure to environmental iodine when foraging on marine/estuarine prey. ...
... Previous research has shown that neonatal alligators from saline habitats at MINWR exhibit a strong correlation between plasma inorganic iodide and the biologically active thyroid hormone, T 3 , which was not observed in the two freshwater populations from the same study (Boggs et al., 2013). This relationship is not present in juvenile alligators from MINWR, as there was no correlation between plasma inorganic iodide and thyroid hormones despite a strong correlations between plasma inorganic iodide and T 3 among the neonatal population (Boggs et al., 2011). ...
... The small adult demographic contains the breeding female population of MINWR which suggests a possible influence of elevated maternal T 3 concentrations on the health of neonates. A previous study demonstrated that neonatal alligators from MINWR had plasma inorganic iodide concentrations that were highly correlated with elevated plasma T 3 concentrations compared to freshwater neonatal counterparts that lacked such correlation (Boggs et al., 2013). This previous study concluded that MINWR neonates demonstrated thyrotoxicosis due to an overproduction of T 3 which was likely due to a maternal over-contribution of iodine or thyroid hormones to the egg for development of the embryo. ...
The American alligator, generally a freshwater species, is known to forage in marine environments despite the lack of a salt secreting gland found in other crocodylids. Estuarine and marine foraging could lead to increased dietary uptake of iodine, a nutrient necessary for the production of thyroid hormones. To explore the influence of dietary iodine on thyroid hormone health of coastal dwelling alligators, we described the seasonal plasma thyroxine and triiodothyronine concentrations measured by radioimmunoassay and urinary iodine (UI) concentrations measured by inductively coupled plasma mass spectrometry. We also analyzed long-term dietary patterns through stable isotope analysis of scute tissue. Snout-to-vent length (SVL) was a significant factor among UI and stable isotope analyses. Large adult males greater than 135 cm SVL had the highest UI concentrations but did not display seasonality of thyroid hormones. Alligators under 135 SVL exhibited seasonality in thyroid hormones and a positive relationship between UI and triiodothyronine concentrations. Isotopic signatures provided supporting evidence that large males predominantly feed on marine/estuarine prey whereas females showed reliance on freshwater/terrestrial prey supplemented by marine/estuarine prey. UI measurement provided immediate information that correlated to thyroid hormone concentrations whereas stable isotope analysis described long-term dietary patterns. Both techniques demonstrate that adult alligators in coastal environments are utilizing estuarine/marine habitats, which could alter thyroid hormone physiology.
