scholarly journals Sexual Development and the Environment: Conclusions from 40 Years of Theory

2021 ◽  
pp. 1-16
Author(s):  
Lisa E. Schwanz ◽  
Arthur Georges

In this review, we consider the insight that has been gained through theoretical examination of environmental sex determination (ESD) and thermolability – how theory has progressed our understanding of the ecological and evolutionary dynamics associated with ESD, the transitional pathways between different modes of sex determination, and the underlying mechanisms. Following decades of theory on the adaptive benefits of ESD, several hypotheses seem promising. These hypotheses focus on the importance of <i>differential fitness</i> (sex-specific effects of temperature on fitness) in generating selection for ESD, but highlight alternative ways differential fitness arises: seasonal impacts on growth, sex-specific ages of maturation, and sex-biased dispersal. ESD has the potential to generate biased sex ratios quite easily, leading to complex feedbacks between the ecology and evolution of ESD. Frequency-dependent selection on sex acts on ESD-related traits, driving local adaptation or plasticity to restore equilibrium sex ratio. However, migration and overlapping generations (“mixing”) diminish local adaptation and leave each cohort/population with the potential for biased sex ratios. Incorporating mechanism into ecology and evolution models reveals similarities between different sex-determining systems. Dosage and gene regulatory network models of sexual development are beginning to shed light on how temperature sensitivity and thresholds may arise. The unavoidable temperature sensitivity in sex-determining systems inherent to these models suggests that evolutionary transitions between genotypic sex determination (GSD) and temperature-dependent sex determination, and between different forms of GSD, are simple and elegant. Theoretical models are often best-served by considering a single piece of a puzzle; however, there is much to gain from reflecting on all of the pieces together in one integrative picture.

Genes ◽  
2020 ◽  
Vol 11 (4) ◽  
pp. 416 ◽  
Author(s):  
Basanta Bista ◽  
Nicole Valenzuela

Sex chromosome evolution remains an evolutionary puzzle despite its importance in understanding sexual development and genome evolution. The seemingly random distribution of sex-determining systems in reptiles offers a unique opportunity to study sex chromosome evolution not afforded by mammals or birds. These reptilian systems derive from multiple transitions in sex determination, some independent, some convergent, that lead to the birth and death of sex chromosomes in various lineages. Here we focus on turtles, an emerging model group with growing genomic resources. We review karyotypic changes that accompanied the evolution of chromosomal systems of genotypic sex determination (GSD) in chelonians from systems under the control of environmental temperature (TSD). These transitions gave rise to 31 GSD species identified thus far (out of 101 turtles with known sex determination), 27 with a characterized sex chromosome system (13 of those karyotypically). These sex chromosomes are varied in terms of the ancestral autosome they co-opted and thus in their homology, as well as in their size (some are macro-, some are micro-chromosomes), heterogamety (some are XX/XY, some ZZ/ZW), dimorphism (some are virtually homomorphic, some heteromorphic with larger-X, larger W, or smaller-Y), age (the oldest system could be ~195 My old and the youngest < 25 My old). Combined, all data indicate that turtles follow some tenets of classic theoretical models of sex chromosome evolution while countering others. Finally, although the study of dosage compensation and molecular divergence of turtle sex chromosomes has lagged behind research on other aspects of their evolution, this gap is rapidly decreasing with the acceleration of ongoing research and growing genomic resources in this group.


2019 ◽  
Vol 157 (1-2) ◽  
pp. 77-88 ◽  
Author(s):  
LingSze Lee ◽  
Eugenia E. Montiel ◽  
Beatriz M. Navarro-Domínguez ◽  
Nicole Valenzuela

Sex-determining mechanisms (SDMs) set an individual's sexual fate by its genotype (genotypic sex determination, GSD) or environmental factors like temperature (temperature- dependent sex determination, TSD), as in turtles where the GSD “trigger” remains unknown. SDMs co-evolve with turtle chromosome number, perhaps because fusions/fissions alter the relative position/regulation of sexual development genes. Here, we map 10 such genes via FISH onto metaphase chromosomes in 6 TSD and 6 GSD turtles for the first time. Results uncovered intrachromosomal rearrangements involving 3 genes across SDMs (Dax1, Fhl2, and Fgf9) and a chromosomal fusion linking 2 genes (Sf1 and Rspo1) in 1 chromosome in a TSD turtle (Pelomedusa subrufa) that locate to 2 chromosomes in all others. Notably, Sf1 and its repressor Foxl2 map to Apalone spinifera's ZW chromosomes but to a macro- (Foxl2) and a microautosome (Sf1) in other turtles potentially inducing SDM evolution. However, our phylogenetically informed analysis refutes Foxl2 (but not Sf1) as Apalone's master sex-determining gene. The absence of common TSD-specific or GSD-specific rearrangements underscores the independent evolutionary trajectories of turtle SDMs. Further comparative analyses using more genes from the sexual development network are warranted to inform genome evolution and its contribution to enigmatic turnovers of vertebrate sex determination.


2017 ◽  
Vol 372 (1729) ◽  
pp. 20160325 ◽  
Author(s):  
Veronika Bókony ◽  
Szilvia Kövér ◽  
Edina Nemesházi ◽  
András Liker ◽  
Tamás Székely

Sex reversals whereby individuals of one genetic sex develop the phenotype of the opposite sex occur in ectothermic vertebrates with genetic sex-determination systems that are sensitive to extreme temperatures during sexual differentiation. Recent rises in global temperatures have led researchers to predict that sex reversals will become more common, resulting in the distortion of many populations' sex ratios. However, it is unclear whether susceptibility to climate-driven sex-ratio shifts depends on the type of sex determination that varies across species. First, we show here using individual-based theoretical models that XX/XY (male-heterogametic) and ZZ/ZW (female-heterogametic) sex-determination systems can respond differentially to temperature-induced sex reversals. Interestingly, the impacts of climate warming on adult sex ratio (ASR) depend on the effects of both genotypic and phenotypic sex on survival and reproduction. Second, we analyse the temporal changes of ASR in natural amphibian populations using data from the literature, and find that ASR shifted towards males in ZZ/ZW species over the past 60 years, but did not change significantly in XX/XY species. Our results highlight the fact that we need a better understanding of the interactions between genetic and environmental sex-determining mechanisms to predict the responses of ectotherms to climate change and the associated extinction risks. This article is part of the themed issue ‘Adult sex ratios and reproductive decisions: a critical re-examination of sex differences in human and animal societies’.


2006 ◽  
Vol 33 (6) ◽  
pp. 475 ◽  
Author(s):  
Arthur Georges ◽  
Fiorenzo Guarino ◽  
Melissa White

Adult sex ratios vary considerably among populations of single species and across years, but the best evidence is drawn from species with temperature-dependent sex determination. It is difficult to disentangle the effects of bias in the production of the sexes and the effects of a range of other factors contributing to biased adult sex ratios. In this paper, we survey sex ratios across populations of a species constrained to produce 1 : 1 offspring sex ratios by genotypic sex determination and show considerable variation in adult sex ratios. Raw adult sex ratios of Emydura macquarii emmottii were significantly biased in nine of the 11 populations examined. In all but one case, the bias was strongly in favour of males. Part of the bias in sex ratio was attributed to the differing ages of maturity of males and females – males mature younger than females – which leads to more male cohorts being included in the calculations of sex ratio than female cohorts. However, correcting for this effect brought the sex ratios of the populations closer to parity, as expected, and accounted for an overall 62% of the male surplus evident in the adult sex ratio. Even so, it was insufficient to explain the strong male bias (1.2–2.9) in five of the nine populations initially showing such bias. This provides support to those who advise caution in interpreting adult sex ratio data for freshwater turtles in the context of demography, sex allocation or evaluating the impact of climate change.


Genes ◽  
2021 ◽  
Vol 12 (2) ◽  
pp. 156
Author(s):  
Lorenzo Clemente ◽  
Sofia Mazzoleni ◽  
Eleonora Pensabene ◽  
Tomáš Protiva ◽  
Philipp Wagner ◽  
...  

The Asian box turtle genus Cuora currently comprises 13 species with a wide distribution in Southeast Asia, including China and the islands of Indonesia and Philippines. The populations of these species are rapidly declining due to human pressure, including pollution, habitat loss, and harvesting for food consumption. Notably, the IUCN Red List identifies almost all species of the genus Cuora as Endangered (EN) or Critically Endangered (CR). In this study, we explore the karyotypes of 10 Cuora species with conventional (Giemsa staining, C-banding, karyogram reconstruction) and molecular cytogenetic methods (in situ hybridization with probes for rDNA loci and telomeric repeats). Our study reveals a diploid chromosome number of 2n = 52 chromosomes in all studied species, with karyotypes of similar chromosomal morphology. In all examined species, rDNA loci are detected at a single medium-sized chromosome pair and the telomeric repeats are restricted to the expected terminal position across all chromosomes. In contrast to a previous report, sex chromosomes are neither detected in Cuoragalbinifrons nor in any other species. Therefore, we assume that these turtles have either environmental sex determination or genotypic sex determination with poorly differentiated sex chromosomes. The conservation of genome organization could explain the numerous observed cases of interspecific hybridization both within the genus Cuora and across geoemydid turtles.


2021 ◽  
Vol 112 (2) ◽  
pp. 155-164
Author(s):  
Suzanne Edmands

Abstract Rising global temperatures threaten to disrupt population sex ratios, which can in turn cause mate shortages, reduce population growth and adaptive potential, and increase extinction risk, particularly when ratios are male biased. Sex ratio distortion can then have cascading effects across other species and even ecosystems. Our understanding of the problem is limited by how often studies measure temperature effects in both sexes. To address this, the current review surveyed 194 published studies of heat tolerance, finding that the majority did not even mention the sex of the individuals used, with &lt;10% reporting results for males and females separately. Although the data are incomplete, this review assessed phylogenetic patterns of thermally induced sex ratio bias for 3 different mechanisms: sex-biased heat tolerance, temperature-dependent sex determination (TSD), and temperature-induced sex reversal. For sex-biased heat tolerance, documented examples span a large taxonomic range including arthropods, chordates, protists, and plants. Here, superior heat tolerance is more common in females than males, but the direction of tolerance appears to be phylogenetically fluid, perhaps due to the large number of contributing factors. For TSD, well-documented examples are limited to reptiles, where high temperature usually favors females, and fishes, where high temperature consistently favors males. For temperature-induced sex reversal, unambiguous cases are again limited to vertebrates, and high temperature usually favors males in fishes and amphibians, with mixed effects in reptiles. There is urgent need for further work on the full taxonomic extent of temperature-induced sex ratio distortion, including joint effects of the multiple contributing mechanisms.


2021 ◽  
Vol 34 (4) ◽  
pp. 594-603
Author(s):  
Gergely Katona ◽  
Balázs Vági ◽  
Zsolt Végvári ◽  
András Liker ◽  
Robert P. Freckleton ◽  
...  

2011 ◽  
Vol 7 (3) ◽  
pp. 443-448 ◽  
Author(s):  
Alexander E. Quinn ◽  
Stephen D. Sarre ◽  
Tariq Ezaz ◽  
Jennifer A. Marshall Graves ◽  
Arthur Georges

Sex in many organisms is a dichotomous phenotype—individuals are either male or female. The molecular pathways underlying sex determination are governed by the genetic contribution of parents to the zygote, the environment in which the zygote develops or interaction of the two, depending on the species. Systems in which multiple interacting influences or a continuously varying influence (such as temperature) determines a dichotomous outcome have at least one threshold. We show that when sex is viewed as a threshold trait, evolution in that threshold can permit novel transitions between genotypic and temperature-dependent sex determination (TSD) and remarkably, between male (XX/XY) and female (ZZ/ZW) heterogamety. Transitions are possible without substantive genotypic innovation of novel sex-determining mutations or transpositions, so that the master sex gene and sex chromosome pair can be retained in ZW–XY transitions. We also show that evolution in the threshold can explain all observed patterns in vertebrate TSD, when coupled with evolution in embryonic survivorship limits.


2018 ◽  
Vol 222 (1) ◽  
pp. jeb190215 ◽  
Author(s):  
Melanie D. Massey ◽  
Sarah M. Holt ◽  
Ronald J. Brooks ◽  
Njal Rollinson

Sign in / Sign up

Export Citation Format

Share Document