Sexual Development and the Environment: Conclusions from 40 Years of Theory (original) (raw)

Sex-Specific Survival to Maturity and the Evolution of Environmental Sex Determination

Evolution, 2016

Four decades ago, it was proposed that environmental sex determination (ESD) evolves when individual fitness depends on the environment in a sex-specific fashion-a form of condition-dependent sex allocation. Many biological processes have been hypothesized to drive this sex asymmetry, yet a general explanation for the evolution of sex-determining mechanisms remains elusive. Here, we develop a mathematical model for a novel hypothesis of the evolution of ESD, and provide a first empirical test using data across turtles. ESD is favored when the sex-determining environment affects annual survival rates equivalently in males and females, and males and females mature at different ages. We compare this hypothesis to alternative hypotheses, and demonstrate how it captures a crucially different process. This maturation process arises naturally from common life histories and applies more broadly to condition-dependent sex allocation. Therefore, it has widespread implications for animal taxa. Across turtle species, ESD is associated with greater sex differences in the age at maturity compared to species without ESD, as predicted by our hypothesis. However, the effect is not statistically significant and will require expanded empirical investigation. Given variation among taxa in sex-specific age at maturity, our survival-to-maturity hypothesis may capture common selective forces on sexdetermining mechanisms.

Climate-driven population divergence in sex-determining systems

Nature, 2010

Sex determination is a fundamental biological process, yet its mechanisms are remarkably diverse 1,2 . In vertebrates, sex can be determined by inherited genetic factors or by the temperature experienced during embryonic development 2,3 . However, the evolutionary causes of this diversity remain unknown. Here we show that live-bearing lizards at different climatic extremes of the species' distribution differ in their sex-determining mechanisms, with temperaturedependent sex determination in lowlands and genotypic sex determination in highlands. A theoretical model parameterized with field data accurately predicts this divergence in sex-determining systems and the consequence thereof for variation in cohort sex ratios among years. Furthermore, we show that divergent natural selection on sex determination across altitudes is caused by climatic effects on lizard life history and variation in the magnitude of between-year temperature fluctuations. Our results establish an adaptive explanation for intra-specific divergence in sex-determining systems driven by phenotypic plasticity and ecological selection, thereby providing a unifying framework for integrating the developmental, ecological and evolutionary basis for variation in vertebrate sex determination.

Mutual information reveals variation in temperature-dependent sex determination in response to environmental fluctuation, lifespan and selection

Proceedings of The Royal Society B: Biological Sciences, 2008

Quantifying the degree to which sex determination depends on the environment can yield insight into the evolution, ecological dynamics, and functional aspects of sex determination. In temperature-dependent sex determination (TSD), theory often predicts a complete dependence of sex on temperature, with a switch-like reaction norm. However, empirical data suggest more shallow relationships between sex and temperature. Here, we demonstrate the usefulness of an index, mutual information (MI), to reflect the degree of temperature dependence in sex. MI depends on both the shape of a reaction norm and the natural temperature variation, thus providing a measure of TSD that is ecologically dependent. We demonstrate that increased lifespan and decreased environmental fluctuation predict reaction norms with high MI (switchlike). However, mutation and weaker selection on sex-specific performance reduce average MI in a population, suggesting that mutation-selection balance can resolve some of the conflict between theoretical predictions of individual-based optimality and population-based empirical results. The MI index allows clear comparison of TSD across life histories and habitats and reveals functional similarities between reaction norms that may appear different. The model provides testable predictions for TSD across populations, namely that MI should increase with lifespan and decrease with historical environmental fluctuations.

SEXUAL SELECTION FAILS TO PROMOTE ADAPTATION TO A NEW ENVIRONMENT

Evolution, 2002

Selection can be divided into sexual and nonsexual components. Some work finds that a component of sexual selection, adaptive female selection for good genes, can promote nonsexual fitness. Less studied is the benefit from sexual selection in toto, that is, when intra-and intersexual selection are both present and able to affect females directly and indirectly. Here an upper bound for the net benefit of sexual selection is estimated for Drosophila melanogaster. Replicate populations were allowed to adapt to low-grade thermal stress, with or with out the operation of sexual selection. Because proteins and lipids are highly sensitive to temperature, low-grade thermal stress will select broadly across the genome for alternative alleles. Such broad, directional selection for thermal tolerance should increase the measurable benefits of sexual selection far beyond that available under stabilizing selection. Sexual selection was removed by enforced monogamy without mate choice and retained by enforced polyandry (four males per female). After 36 generations of thermal stress exposure, there was substantial adaptation to the new environment (the net reproductive rate increased six standard deviations relative to thermal controls). However, sexual selection did not affect the rate of adaptation. Therefore, adaptive female selection for thermal tolerance either was insignificant or negated by other aspects of sexual selection, for example, male-induced female harm, which has been shown to diminish under monogamy. This experiment employed two parameters that reduced the opportunity for divergence in such harm: a truncated intersexual interaction period and strong directional selection for thermal tolerance. No divergence in male-induced harm was observed.

Temperature-dependent sex determination and global change: are some species at greater risk?

Oecologia, 2009

In species with temperature-dependent sex determination (TSD), global climate change may result in a strong sex ratio bias that could lead to extinction. The relationship between sex ratio and egg incubation at constant temperature in TSD species is characterized by two parameters: the pivotal temperature (P) and the transitional range of temperature that produces both sexes (TRT). Here, we show that the proportion of nests producing both sexes is positively correlated to the width of the TRT by a correlative approach from sex ratio data collected in the literature and by simulations of TSD using a mechanistic model. From our analyses, we predict that species with a larger TRT should be more likely to evolve in response to new thermal conditions, thus putting them at lower risk to global change.

Male-limited secondary sexual trait interacts with environment in determining female fitness

Evolution, 2018

Selection for secondary sexual trait (SST) elaboration may increase intralocus sexual conflict over the optimal values of traits expressed from shared genomes. This conflict can reduce female fitness, and the resulting gender load can be exacerbated by environmental stress, with consequences for a population's ability to adapt to novel environments. However, how the evolution of SSTs interacts with environment in determining female fitness is not well understood. Here, we investigated this question using replicate lines of bulb mites selected for increased or decreased prevalence of a male SST-thickened legs used as weapons. The fitness of females from these lines was measured at a temperature to which the mites were adapted (24°C), as well as at two novel temperatures: 18°C and 28°C. We found the prevalence of the SST interacted with temperature in determining female fecundity. At 28°C, females from populations with high SST prevalence were less fecund than females from populations in which the SST was rare, but the reverse was true at 18°C. Thus, a novel environment does not universally depress female fitness more in populations with a high degree of sexually selected dimorphism. We discuss possible consequences of the interaction we detected for adaptation to novel environments.

Temperature-Dependent Sex Determination and Contemporary Climate Change

Sexual Development, 2010

management should aim to neutralise directional sex ratio biases (e.g. by manipulating incubation temperatures or assisted migration) and promote adaptive processes, possibly by genetic supplementation of populations. These practices should aid species' persistence and buy time for research directed at more accurate prediction of species' vulnerability.

Sexual selection in complex environments

2014

Sexual selection has resulted in some of the most captivating features of insects, including flashy colors, bizarre structures, and complex pheromones. These features evolve in dynamic environments, where conditions can change rapidly over space and time. However, only recently has ecological complexity been embraced by theory and practice in sexual selection. We review replicated selection studies as well as studies on variation in the agents of selection to delineate gaps in current knowledge and clarify exciting new directions for research. Existing work suggests that fluctuations in sexual selection may be extremely common, though work on the ecological factors influencing these fluctuations is scarce. We suggest that deeper ecological perspectives on sexual selection may alter some of the fundamental assumptions of sexual selection theory and rapidly lead to new discoveries.