Temperature-Dependent Sex Determination in Fish Revisited: Prevalence, a Single Sex Ratio Response Pattern, and Possible Effects of Climate Change

Abstract

BackgroundIn gonochoristic vertebrates, sex determination mechanisms can be classified as genotypic (GSD) or temperature-dependent (TSD). Some cases of TSD in fish have been questioned, but the prevalent view is that TSD is very common in this group of animals, with three different response patterns to temperature.Methodology/Principal FindingsWe analyzed field and laboratory data for the 59 fish species where TSD has been explicitly or implicitly claimed so far. For each species, we compiled data on the presence or absence of sex chromosomes and determined if the sex ratio response was obtained within temperatures that the species experiences in the wild. If so, we studied whether this response was statistically significant. We found evidence that many cases of observed sex ratio shifts in response to temperature reveal thermal alterations of an otherwise predominately GSD mechanism rather than the presence of TSD. We also show that in those fish species that actually have TSD, sex ratio response to increasing temperatures invariably results in highly male-biased sex ratios, and that even small changes of just 1–2°C can significantly alter the sex ratio from 1∶1 (males∶females) up to 3∶1 in both freshwater and marine species.Conclusions/SignificanceWe demonstrate that TSD in fish is far less widespread than currently believed, suggesting that TSD is clearly the exception in fish sex determination. Further, species with TSD exhibit only one general sex ratio response pattern to temperature. However, the viability of some fish populations with TSD can be compromised through alterations in their sex ratios as a response to temperature fluctuations of the magnitude predicted by climate change.

Heat-induced masculinization in domesticated zebrafish is family-specific and yields a set of different gonadal transcriptomes

“…In agreement with the general pattern in fish (18), elevated temperatures result in a higher number of males, although, surprisingly, one study reported more females (40). However, most of the above experiments involved progeny derived from a single family, mixtures of several broods, low sample sizes, or offspring from gynogenetic parents, the latter raising the possibility of unaccounted effects of inbreeding.…”

“…Regardless of the actual underlying sex-determining mechanism, a shared characteristic of all fish species in which temperature can alter sex ratios is that exposure to heat during early development upregulates the expression of genes related to testis differentiation with a concomitant down-regulation of genes related to ovarian differentiation, as assessed in several species (e.g., 9,13,[15][16][17]. This results in an increase in the proportion of males (18) and implies that some genetic females (XX or ZW females) in CSD species, or fish that otherwise would develop as females in a PSD system, end up developing as phenotypic males despite their genetic makeup. These masculinized or sex-reversed females are called "neomales," and have testicular structure (19) and gene expression profiles similar or identical to those of males (20,21) and can produce viable sperm.…”

Climate change and pollution speed declines in zebrafish populations

“…Female-biased populations are not necessarily at greater risk of extinction, provided some males are present (19), since numbers of females, rather than males, largely determine the reproductive output of a population (19,20). However, in lizards (17,18), fish (21), and some amphibians (22), temperature elevation tends to induce male development and male-biased sex ratios can dramatically reduce population fitness (23,24). Sexual differentiation in these animals is also strongly influenced by chemicals that disrupt hormone systems (25)(26)(27)(28).…”

“…The zebrafish is a freshwater species native to the Indian subcontinent and has been studied widely as a model animal in biomedical and environmental science (36)(37)(38). Importantly, the sex-determining mechanism in zebrafish is known to be modified by environmental factors, and independent exposures to elevated water temperatures (21,39), and to chemicals that inhibit aromatase, have been shown to induce male development in this species (39,40). The enzyme aromatase [cytochrome P450(CYP)19] mediates the conversion of male hormones (androgens) to female hormones (estrogens), and thus plays a pivotal role in sex assignment in zebrafish and other vertebrates (41).…”

Reproductive biology of the Indian scad, Decapterus russelli (Ruppell, 1830) from Maharashtra waters, northwest coast of India

“…Month wise distribution of sex-ratio indicated significant predominance of male at 5% in April, May and November, whereas the total sex-ratio over the year was significantly male dominated at 5% level. Since the reproductive potential of many fish communities is determined by the number of females available for egg production highly male-biased sex-ratios would likely affect population structure and the viability of sensitive stocks (Ospina and Piferrer, 2008). Slightly higher ratio in the present study is not likely to affect the future population as highest numbers of females were seen in the …”