Temperature-dependent sex determination in fish revisited: prevalence, a single sex ratio response pattern, and possible effects of climate change

Abstract

Background: In 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 findings: We 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 degrees C can significantly alter the sex ratio from 1:1 (males:females) up to 3:1 in both freshwater and marine species.

Conclusions/significance: We 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.

Figure 1. Patterns of temperature-dependent sex determination (TSD) in fish that had been recognized to date.

They are defined according to the sex ratio produced as a function of temperature during the thermosensitive period. A, Pattern 1, low temperatures produce female-biased sex ratios and high temperatures produce male-biased sex ratios. B, Pattern 2, low temperatures produce male-biased sex ratios and high temperatures produce female-biased sex ratios. C, Pattern 3, male-biased sex ratios are produced at low and high temperatures, while balanced sex ratios are produced at intermediate temperatures. In some cases, the response may be partial (dashed line in A). The present study demonstrates that fish species with TSD only exhibit pattern 1.

Figure 2. Set of criteria used to determine the presence of temperature-dependent sex determination (TSD) as opposed to genotypic sex determination (GSD), and to distinguish TSD from thermal effects on GSD (GSD+TE).

This algorithm is based on the criteria of Valenzuela et al. (2003), and incorporates a modification of the criteria of Conover (2004). See text in the Materials and Methods section for a complete explanation. *Indicates that the evidence for a sex chromosomal system may come from direct (karyotyping, banding) or indirect methods (e.g., progeny analysis of sex-linked traits, mating experiments or crosses with sex-reversed fish). **Indicates that the sex ratio shift must occur within the range of developmental temperatures during development that includes the thermosensitive period (RTD) regardless of whether there is response within the range of natural temperatures where the species lives.

Figure 3. Patterns of sex ratio response to temperature in fish.

A, Examples of authentic cases of TSD following pattern 1, more males with increasing temperatures. Sex ratio shifts occur within the range of temperature (shaded areas) normally experienced by fish in the wild. B, Examples of false cases of TSD. Sex ratio shifts only occur at extreme temperatures, and thus represent thermal effects on GSD (a, b). Formerly proposed pattern 2 (c), fewer males at high temperature, is not supported by re-analysis of data (see also Supplementary Table 1). C, Formerly proposed pattern 3, more males at extreme temperatures, can be explained from the combination of two effects unrelated to TSD: slow growing fish at low temperature differentiating as males (a), and the inhibition of aromatase at high temperature causing sex-reversal of genetic females (b). When combined, the two effects result in the observed pattern (c).

Figure 4. Patterns of sex ratio response to temperature in species of fish with TSD.

In all cases, higher temperatures imply a higher number of males produced. Key: 1, Mendia menidia; 2, Odontesthes bonariensis; 3, Hoplosternum littorale; 4, Poeciliopsis lucida; 5, average of the 33 Apistogramma species; 6, Limia melanogaster; 7, Menidia peninsulae; 8, Odontesthes argentinensis.

Figure 5. Distribution of temperature-dependent sex determination (TSD) in fish.

Orders, families and species with TSD are marked in color. Teleost phylogeny based on Nelson .