Thyroid hormone modulates offspring sex ratio in a turtle with temperature-dependent sex determination

The adaptive significance of temperature-dependent sex determination (TSD) has attracted a great deal of research, but the underlying mechanisms by which temperature determines the sex of a developing embryo remain poorly understood. Here, we manipulated the level of a thyroid hormone (TH), triiodothyronine (T 3 ), during embryonic development (by adding excess T 3 to the eggs of the red-eared slider turtle Trachemys scripta , a reptile with TSD), to test two competing hypotheses on the proximate basis for TSD: the developmental rate hypothesis versus the hormone hypothesis . Exogenous TH accelerated embryonic heart rate (and hence metabolic rate), developmental rate, and rates of early post-hatching growth. More importantly, hyperthyroid conditions depressed expression of Cyp19a1 (the gene encoding for aromatase) and levels of oestradiol, and induced more male offspring. This result is contrary to the direction of sex-ratio shift predicted by the developmental rate hypothesis , but consistent with that predicted by the hormone hypothesis . Our results suggest an important role for THs in regulating sex steroid hormones, and therefore, in affecting gonadal sex differentiation in TSD reptiles. Our study has implications for the conservation of TSD reptiles in the context of global change because environmental contaminants may disrupt the activity of THs, and thereby affect offspring sex in TSD reptiles.

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Does sex-ratio selection influence nest-site choice in a reptile with temperature-dependent sex determination?

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2013.2460 ◽

2013 ◽

Vol 280 (1772) ◽

pp. 20132460 ◽

Cited By ~ 33

Author(s):

Timothy S. Mitchell ◽

Jessica A. Maciel ◽

Fredric J. Janzen

Keyword(s):

Sex Ratio ◽

Sex Determination ◽

Nest Site ◽

Sex Ratios ◽

Temperature Dependent ◽

Dioecious Species ◽

Offspring Sex Ratio ◽

Nest Sites ◽

Offspring Sex ◽

Nest Site Choice

Evolutionary theory predicts that dioecious species should produce a balanced primary sex ratio maintained by frequency-dependent selection. Organisms with environmental sex determination, however, are vulnerable to maladaptive sex ratios, because environmental conditions vary spatio-temporally. For reptiles with temperature-dependent sex determination, nest-site choice is a behavioural maternal effect that could respond to sex-ratio selection, as mothers could adjust offspring sex ratios by choosing nest sites that will have particular thermal properties. This theoretical prediction has generated decades of empirical research, yet convincing evidence that sex-ratio selection is influencing nesting behaviours remains absent. Here, we provide the first experimental evidence from nature that sex-ratio selection, rather than only viability selection, is probably an important component of nest-site choice in a reptile with temperature-dependent sex determination. We compare painted turtle ( Chrysemys picta ) neonates from maternally selected nest sites with those from randomly selected nest sites, observing no substantive difference in hatching success or survival, but finding a profound difference in offspring sex ratio in the direction expected based on historical records. Additionally, we leverage long-term data to reconstruct our sex ratio results had the experiment been repeated in multiple years. As predicted by theory, our results suggest that sex-ratio selection has shaped nesting behaviour in ways likely to enhance maternal fitness.

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Conservation of sex-linked markers among conspecific populations of a viviparous skink, Niveoscincus ocellatus, exhibiting genetic and temperature dependent sex determination

10.1101/257428 ◽

2018 ◽

Author(s):

Peta Hill ◽

Christopher P. Burridge ◽

Tariq Ezaz ◽

Erik Wapstra

Keyword(s):

Linkage Disequilibrium ◽

Sex Ratio ◽

Sex Determination ◽

Temperature Dependent ◽

Offspring Sex Ratio ◽

Evolutionary Transitions ◽

Offspring Sex ◽

Determination System ◽

Sex Determination System ◽

Male Heterogamety

AbstractSex determination systems are exceptionally diverse and have undergone multiple and independent evolutionary transitions among species, particularly reptiles. However, the mechanisms underlying these transitions have not been established. Here we tested for differences in sex-linked markers in the only known reptile that is polymorphic for sex determination system, the spotted snow skink, Niveoscincus ocellatus, to quantify the genomic differences that have accompanied this transition. In a highland population, sex is determined genetically, whilst in a lowland population, offspring sex ratio is influenced by temperature. We found a similar number of sex-linked loci in each population, including shared loci, with genotypes consistent with male heterogamety (XY). However, population-specific linkage disequilibrium suggests greater divergence of sex chromosomes in the highland population. Our results suggest that transitions between sex determination systems (GSD and TSD-like systems) can be facilitated by subtle genetic differences.

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Transgenerational sex determination: the embryonic environment experienced by a male affects offspring sex ratio

Scientific Reports ◽

10.1038/srep02709 ◽

2013 ◽

Vol 3 (1) ◽

Cited By ~ 22

Author(s):

Daniel A. Warner ◽

Tobias Uller ◽

Richard Shine

Keyword(s):

Sex Ratio ◽

Sex Determination ◽

Offspring Sex Ratio ◽

Offspring Sex

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Intraspecific genome size variation in a turtle (Trachemys scripta) exhibiting temperature-dependent sex determination

Canadian Journal of Zoology ◽

10.1139/z91-324 ◽

1991 ◽

Vol 69 (9) ◽

pp. 2306-2310 ◽

Cited By ~ 10

Author(s):

Samuel F. Lockwood ◽

Brenden S. Holland ◽

John W. Bickham ◽

Brian G. Hanks ◽

James J. Bull

Keyword(s):

Sex Ratio ◽

Sex Determination ◽

Genome Size ◽

Incubation Temperature ◽

Size Variation ◽

Developmental Rate ◽

Trachemys Scripta ◽

Temperature Dependent ◽

Genome Size Variation ◽

Different Temperatures

Variation in genome size within and among populations of the pond slider, Trachemys scripta, a species with temperature-dependent sex determination, was investigated. Because genome size has been shown to affect developmental rate in various organisms, as does incubation temperature, it was hypothesized that genome size could influence sex determination in species with environmental sex determination. Significant variation in DNA content was found between geographic populations and among clutches. No significant differences in mean genome size were observed among samples incubated at different temperatures or between sexes of turtles hatched at a temperature that yields a mixed sex ratio. Thus, it appears that sex determination in T. scripta is accomplished in the absence of sex-specific and incubation-temperature-specific differences in genome size. Preliminary data from two populations, however, suggest that genome size may be significantly correlated with the threshold incubation temperature at which a mixed sex ratio is produced.

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Endogenous Corticosterone Elevations Five Hours Prior to Ovulation do not Influence Offspring Sex Ratios in Zebra Finches

Avian Biology Research ◽

10.3184/175815516x14495923605779 ◽

2016 ◽

Vol 9 (3) ◽

pp. 131-138 ◽

Cited By ~ 1

Author(s):

A.E. Gam ◽

K.J. Navara

Keyword(s):

Sex Ratio ◽

Sex Ratios ◽

Zebra Finches ◽

Meiotic Segregation ◽

Offspring Sex Ratio ◽

Handling Stress ◽

Offspring Sex ◽

Baseline Corticosterone ◽

Underlying Mechanisms ◽

Heterogametic Sex

Previous research suggests that environmental and social factors can drive female birds to bias offspring sex ratios. The underlying mechanisms controlling these adjustments remain unclear. Results from experimental and correlative research suggest that maternal corticosterone plays an important role in this process. Since females are the heterogametic sex in birds, corticosterone may potentially bias offspring sex ratios during meiotic segregation, through non-random segregation of sex chromosomes. In a previous study, we showed that pharmacological elevations of corticosterone near the time of meiotic segregation exerted an effect on offspring sex ratio, causing female Zebra Finches ( Taeniopygia guttata) to produce significantly more males. Here, we aimed to determine whether endogenous elevations in the physiological range have similar effects on offspring sex. First we examined offspring sex ratio in relation to baseline corticosterone levels to determine if natural variation in circulating corticosterone near the time of meiotic segregation is related to offspring sex ratio. Next, we used a 5-minute bag handling protocol to induce corticosterone elevations 5 hours prior to ovulation. Maternal baseline corticosterone levels did not correlate with average clutch sex ratios. In addition, the sex ratios produced by females exposed to handling stress did not differ from sex ratios produced by unmanipulated females. Together these results suggest that physiological levels of endogenous corticosterone, both baseline and acutely elevated near the time of sex determination may not be involved in the adjustment of primary sex ratios in Zebra Finches.

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Skewed Sex-Ratio, Monogeny, and Maternal Sex Determination in Two Geographical Populations of Asellus Aquaticus (L., 1758) (Isopoda)

Crustaceana ◽

10.1163/156854096x01041 ◽

1996 ◽

Vol 69 (4) ◽

pp. 455-475 ◽

Cited By ~ 5

Author(s):

Giovanna Vitagliano ◽

Enzo Marchetti ◽

Eleonora Vitagliano

Keyword(s):

Sex Ratio ◽

Sex Determination ◽

The Other ◽

Italian Population ◽

Asellus Aquaticus ◽

Offspring Sex Ratio ◽

New Born ◽

Offspring Sex ◽

Geographical Populations ◽

Biased Sex Ratio

AbstractFor the great majority of the amphipods and isopods a biased sex ratio is attributed to photoperiod or to micro-organisms present in the cytoplasm of the oocytes. Since monogenous pairs are found in orders and species phylogenetically very far from each other, in order to try and clarify this phenomenon, two geographical populations of Asellus aquaticus (Isopoda) were collected in the Netherlands and in Italy, where the duration of the cold season and the photoperiods are very different. From these parental (P) populations, 200 females and 200 males per population were randomly subsampled and bred under standard conditions of temperature and nutrition. One half of each P generation was subjected to 18 hours light per day, the other to 14 hours light per day. New-born of each pair (laboratory F1) were grown up to differentiation of external sexual characters under the same photoperiod experienced by the parents. Also, hybrid F1 generation, born from mating between the two populations, was conceived in both photoperiods, but, after birth, one half of the new-born was maintained in the same photoperiod in which they were conceived, the other half was grown under the other photoperiod. No significant difference between the sex ratios was found in the two photoperiods, neither between Italian nor between Dutch Asellus. The sex ratio of Dutch F1 is female biased, while it is male biased in Italian Asellus. The female- or male-biased sex ratio can be ascribed to the high proportion of monogenous pairs in which offspring sex ratio is significantly biased towards females (in the Dutch population) and/or in which offspring sex ratio is significantly biased towards males (in the Italian population). On the basis of these results we can rule out the influence of photoperiod in sex determination for this species. The results shown by the hybrids suggest some form of maternal inheritance. In fact, the hybrids' sex ratio as indeed the frequency of pairs breeding one sex alone, was skewed towards the same sex for which the maternal population showed a bias. We therefore consider the possibility of sex determination associated with a cytoplasmic factor (a mitochondrial DNA?), which would inactivate only one of the two sets of genes governing sex determination.

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Transgenerational epigenetic sex determination: Environment experienced by female fish affects offspring sex ratio

Environmental Pollution ◽

10.1016/j.envpol.2021.116864 ◽

2021 ◽

Vol 277 ◽

pp. 116864

Author(s):

Fabien Pierron ◽

Sophie Lorioux ◽

Débora Héroin ◽

Guillemine Daffe ◽

Bruno Etcheverria ◽

...

Keyword(s):

Sex Ratio ◽

Sex Determination ◽

Female Fish ◽

Offspring Sex Ratio ◽

Offspring Sex

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Meiotic drive and sex determination: molecular and cytological mechanisms of sex ratio adjustment in birds

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2007.0006 ◽

2007 ◽

Vol 363 (1497) ◽

pp. 1675-1686 ◽

Cited By ~ 98

Author(s):

Joanna Rutkowska ◽

Alexander V Badyaev

Keyword(s):

Sex Ratio ◽

Sex Determination ◽

Sex Chromosomes ◽

Sex Ratios ◽

Relative Fitness ◽

Compensatory Mechanisms ◽

Offspring Sex Ratio ◽

Epigenetic Effects ◽

Offspring Sex ◽

Sex Ratio Adjustment

Differences in relative fitness of male and female offspring across ecological and social environments should favour the evolution of sex-determining mechanisms that enable adjustment of brood sex ratio to the context of breeding. Despite the expectation that genetic sex determination should not produce consistent bias in primary sex ratios, extensive and adaptive modifications of offspring sex ratio in relation to social and physiological conditions during reproduction are often documented. Such discordance emphasizes the need for empirical investigation of the proximate mechanisms for modifying primary sex ratios, and suggests epigenetic effects on sex-determining mechanisms as the most likely candidates. Birds, in particular, are thought to have an unusually direct opportunity to modify offspring sex ratio because avian females are heterogametic and because the sex-determining division in avian meiosis occurs prior to ovulation and fertilization. However, despite evidence of strong epigenetic effects on sex determination in pre-ovulatory avian oocytes, the mechanisms behind such effects remain elusive. Our review of molecular and cytological mechanisms of avian meiosis uncovers a multitude of potential targets for selection on biased segregation of sex chromosomes, which may reflect the diversity of mechanisms and levels on which such selection operates in birds. Our findings indicate that pronounced differences between sex chromosomes in size, shape, size of protein bodies, alignment at the meiotic plate, microtubule attachment and epigenetic markings should commonly produce biased segregation of sex chromosomes as the default state, with secondary evolution of compensatory mechanisms necessary to maintain unbiased meiosis. We suggest that it is the epigenetic effects that modify such compensatory mechanisms that enable context-dependent and precise adjustment of primary sex ratio in birds. Furthermore, we highlight the features of avian meiosis that can be influenced by maternal hormones in response to environmental stimuli and may account for the precise and adaptive patterns of offspring sex ratio adjustment observed in some species.

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Periconceptional influences on offspring sex ratio and placental responses

Reproduction Fertility and Development ◽

10.1071/rd11906 ◽

2012 ◽

Vol 24 (1) ◽

pp. 45 ◽

Cited By ~ 24

Author(s):

Cheryl S. Rosenfeld

Keyword(s):

Gene Expression ◽

Sex Ratio ◽

Maternal Diet ◽

Expression Patterns ◽

Offspring Sex Ratio ◽

Biological Responses ◽

Increased Risk ◽

Offspring Sex ◽

Secondary Sex Ratio ◽

Underlying Mechanisms

Maternal diet and secondary factors can strikingly influence fetal outcomes, including biasing offspring sex ratio and altering the molecular biological responses of the conceptus, namely within the placenta. Alterations in the in utero environment might also lead to profound developmental origin of health and disease (DOHaD) outcomes into adulthood, including increased risk for cardiovascular disease, obesity and cancer, with males in general being at greater risk for these diseases. Female mice maintained on a very high fat (VHF) diet birth more sons than those on a chow-based and low fat (LF), high carbohydrate diet, with the latter group producing more daughters. However, neither the underlying mechanisms that contribute to this shift in offspring sex ratio nor when they occur during pregnancy have been resolved. In this review, we consider the evidence that maternal diet and other factors influence secondary sex ratio in a variety of species, including humans, and discuss when this skewing might occur. Additionally, we examine how fetal sex and maternal diet influences gene expression patterns in the mouse placenta, which serves as the primary nutrient acquisition and communication organ between the mother and her developing pups. These adaptations to diet observed as changes in gene expression are likely to provide insight into how the placenta buffers the fetus proper from environmental shifts in nutrient availability during pregnancy and whether male and female conceptuses respond differently to such challenges.

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