The influence of thermal signals during embryonic development on intrasexual and sexually dimorphic gene expression and circulating steroid hormones in American alligator hatchlings (Alligator mississippiensis)

McCoy, Jessica A.; Hamlin, Heather J.; Thayer, LeeAnne; Guillette, Louis J.; Parrott, Benjamin B.

doi:10.1016/j.ygcen.2016.04.011

Cited by 11 publications

(20 citation statements)

References 24 publications

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“…Expression of aromatase, the enzyme that produces estrogen, has been hypothesized to be a master regulator of sex-biased gene expression in developing alligator embryos (Lance 2009) because of the ability of estrogen exposure to cause sex reversal in embryos incubated at MPT (Bull et al 1988) and its extreme sex-biased expression in embryonic gonads after TSP (Gabriel et al 2001). While much work is currently being performed to determine the pathway that allows aromatase expression to vary with temperature (Parrott et al 2014;Yatsu et al 2015;McCoy et al 2016), less attention has been paid to the questions of which genes estrogen regulates during sexual development in American alligators or how estrogen regulates them despite its pivotal role early in embryonic sexual differentiation in alligators. Our data do not speak to the hypothesis that TRPV4 is a component of the temperaturesensing apparatus responsible for TSD (Yatsu et al 2015) as we find no evidence of expression of this gene in any tissue at any of our time points.…”

Section: Discussionmentioning

confidence: 99%

“…Much work has been performed in alligators and other vertebrates with TSD to determine the initial switch that links temperature to sexual fate (Kohno et al 2010;Schroeder et al 2016) and the cause of increased expression of aromatase at FPT (Parrott et al 2014;McCoy et al 2016). One recent hypothesis for the gene acting as the initial switch in the American alligator is the thermosensitive TRP channel TRPV4, as it is activated at temperatures near MPT in vitro and targets gene expression of male development genes (Yatsu et al 2015).…”

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confidence: 99%

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Improved genome assembly of American alligator genome reveals conserved architecture of estrogen signaling

Rice

Kohno

John³

et al. 2017

Genome Res.

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The American alligator, , like all crocodilians, has temperature-dependent sex determination, in which the sex of an embryo is determined by the incubation temperature of the egg during a critical period of development. The lack of genetic differences between male and female alligators leaves open the question of how the genes responsible for sex determination and differentiation are regulated. Insight into this question comes from the fact that exposing an embryo incubated at male-producing temperature to estrogen causes it to develop ovaries. Because estrogen response elements are known to regulate genes over long distances, a contiguous genome assembly is crucial for predicting and understanding their impact. We present an improved assembly of the American alligator genome, scaffolded with in vitro proximity ligation (Chicago) data. We use this assembly to scaffold two other crocodilian genomes based on synteny. We perform RNA sequencing of tissues from American alligator embryos to find genes that are differentially expressed between embryos incubated at male- versus female-producing temperature. Finally, we use the improved contiguity of our assembly along with the current model of CTCF-mediated chromatin looping to predict regions of the genome likely to contain estrogen-responsive genes. We find that these regions are significantly enriched for genes with female-biased expression in developing gonads after the critical period during which sex is determined by incubation temperature. We thus conclude that estrogen signaling is a major driver of female-biased gene expression in the post-temperature sensitive period gonads.

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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

Improved genome assembly of American alligator genome reveals conserved architecture of estrogen signaling

Rice

Kohno

John³

et al. 2017

Genome Res.

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“…In these species, the temperature embryos experience during incubation determines whether they develop as male or female [6][7][8]. As a result, thermal regimes associated with climate change have the potential to profoundly impact population sex ratios as well as inter-and intrasexual variation [9,10]. Such skews in population sex ratios can threaten population persistence, and even lead to local extinctions via reduced effective population size and mate limitation [11,12].…”

Section: Introductionmentioning

confidence: 99%

Spatial and temporal variation in nest temperatures forecasts sex ratio skews in a crocodilian with environmental sex determination

et al. 2020

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Species displaying temperature-dependent sex determination (TSD) are especially vulnerable to the effects of a rapidly changing global climate due to their profound sensitivity to thermal cues during development. Predicting the consequences of climate change for these species, including skewed offspring sex ratios, depends on understanding how climatic factors interface with features of maternal nesting behaviour to shape the developmental environment. Here, we measure thermal profiles in 86 nests at two geographically distinct sites in the northern and southern regions of the American alligator's ( Alligator mississippiensis ) geographical range, and examine the influence of both climatic factors and maternally driven nest characteristics on nest temperature variation. Changes in daily maximum air temperatures drive annual trends in nest temperatures, while variation in individual nest temperatures is also related to local habitat factors and microclimate characteristics. Without any compensatory nesting behaviours, nest temperatures are projected to increase by 1.6–3.7°C by the year 2100, and these changes are predicted to have dramatic consequences for offspring sex ratios. Exact sex ratio outcomes vary widely depending on site and emission scenario as a function of the unique temperature-by-sex reaction norm exhibited by all crocodilians. By revealing the ecological drivers of nest temperature variation in the American alligator, this study provides important insights into the potential consequences of climate change for crocodilian species, many of which are already threatened by extinction.

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“…While much work is currently being performed to determine the pathway that allows aromatase expression to vary with temperature (Parrott et al 2014;Yatsu et al 2015;McCoy et al 2016), less attention has been paid to the questions of which genes estrogen regulates during sexual development in American alligators or how estrogen regulates them despite its pivotal role early in embryonic sexual differentiation in alligators. Our data do not speak to the hypothesis that TRPV4 is a component of the temperaturesensing apparatus responsible for TSD (Yatsu et al 2015) as we find no evidence of expression of this gene in any tissue at any of our time points.…”

Section: Discussionmentioning

confidence: 99%

Improved genome assembly of American alligator genome reveals conserved architecture of estrogen signaling

Rice

Kohno

John³

et al. 2016

Preprint

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The American alligator, Alligator mississippiensis, like all crocodilians, has temperature-dependent sex determination, in which the sex of an embryo is determined by the incubation temperature of the egg during a critical period of development. The lack of genetic differences between male and female alligators leaves open the question of how the genes responsible for sex determination and differentiation are regulated. Insight into this question comes from the fact that exposing an embryo incubated at male-producing temperature to estrogen causes it to develop ovaries. Because estrogen response elements are known to regulate genes over long distances, a contiguous genome assembly is crucial for predicting and understanding their impact. We present an improved assembly of the American alligator genome, scaffolded with in vitro proximity ligation (Chicago) data. We use this assembly to scaffold two other crocodilian genomes based on synteny. We perform RNA sequencing of tissues from American alligator embryos to find genes that are differentially expressed between embryos incubated at male-versus female-producing temperature. Finally, we use the improved contiguity of our assembly along with the current model of CTCF-mediated chromatin looping to predict regions of the genome likely to contain estrogen-responsive genes. We find that these regions are significantly enriched for genes with female-biased expression in developing gonads after the critical period during which sex is determined by incubation temperature. We thus conclude that estrogen signaling is a major driver of female-biased gene expression in the post-temperature sensitive period gonads.

show abstract

The influence of thermal signals during embryonic development on intrasexual and sexually dimorphic gene expression and circulating steroid hormones in American alligator hatchlings (Alligator mississippiensis)

Cited by 11 publications

References 24 publications

Improved genome assembly of American alligator genome reveals conserved architecture of estrogen signaling

Improved genome assembly of American alligator genome reveals conserved architecture of estrogen signaling

Spatial and temporal variation in nest temperatures forecasts sex ratio skews in a crocodilian with environmental sex determination

Improved genome assembly of American alligator genome reveals conserved architecture of estrogen signaling

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