Population consequences of environmental sex reversal.

When sex determination in a species is predominantly genetic but environmentally reversible, exposure to (anthropogenic) changes in the environment can lead to shifts in a population's sex ratio. Such scenarios may be common in many fishes and amphibians, yet their ramifications remain largely unexplored. We used a simple model to study the (short-term) population consequences of environmental sex reversal (ESR). We examined the effects on sex ratios, sex chromosome frequencies, and population growth and persistence after exposure to environmental forces with feminizing or masculinizing tendencies. When environmental feminization was strong, X chromosomes were driven to extinction. Analogously, extinction of normally male-linked genetic factors (e.g., Y chromosomes) was caused by continuous environmental masculinization. Although moderate feminization was beneficial for population growth in the absence of large viability effects, our results suggest that the consequences of ESR are generally negative in terms of population size and the persistence of sex chromosomes. Extreme sex ratios resulting from high rates of ESR also reduced effective population sizes considerably. This may limit any evolutionary response to the deleterious effects of ESR. Our findings suggest that ESR changes population growth and sex ratios in some counter-intuitive ways and can change the predominant factor in sex determination from genetic to fully environmental, often within only a few tens of generations. Populations that lose genetic sex determination may quickly go extinct if the environmental forces that cause sex reversal cease.

Searching for sex-reversals to explain population demography and the evolution of sex chromosomes.

Sex determination can be purely genetic (as in mammals and birds), purely environmental (as in many reptiles), or genetic but reversible by environmental factors during a sensitive period in life, as in many fish and amphibians (Wallace et al. 1999; Baroiller et al. 2009a; Stelkens & Wedekind 2010). Such environmental sex reversal (ESR) can be induced, for example, by temperature changes or by exposure to hormone-active substances. ESR has long been recognized as a means to produce more profitable single-sex cultures in fish farms (Cnaani & Levavi-Sivan 2009), but we know very little about its prevalence in the wild. Obviously, induced feminization or masculinization may immediately distort population sex ratios, and distorted sex ratios are indeed reported from some amphibian and fish populations (Olsen et al. 2006; Alho et al. 2008; Brykov et al. 2008). However, sex ratios can also be skewed by, for example, segregation distorters or sex-specific mortality. Demonstrating ESR in the wild therefore requires the identification of sex-linked genetic markers (in the absence of heteromorphic sex chromosomes) followed by comparison of genotypes and phenotypes, or experimental crosses with individuals who seem sex reversed, followed by sexing of offspring after rearing under non-ESR conditions and at low mortality. In this issue, Alho et al. (2010) investigate the role of ESR in the common frog (Rana temporaria) and a population that has a distorted adult sex ratio. They developed new sex-linked microsatellite markers and tested wild-caught male and female adults for potential mismatches between phenotype and genotype. They found a significant proportion of phenotypic males with a female genotype. This suggests environmental masculinization, here with a prevalence of 9%. The authors then tested whether XX males naturally reproduce with XX females. They collected egg clutches and found that some had indeed a primary sex ratio of 100% daughters. Other clutches seemed to result from multi-male fertilizations of which at least one male had the female genotype. These results suggest that sex-reversed individuals affect the sex ratio in the following generation. But how relevant is ESR if its prevalence is rather low, and what are the implications of successful reproduction of sex-reversed individuals in the wild?