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

Ospina-Alvarez N, Piferrer F - PLoS ONE (2008)

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Institut de Ciències del Mar, Consejo Superior de Investigaciones Científicas, Barcelona, Spain.

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.

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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).
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pone-0002837-g003: 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).

Mentions: To determine the actual prevalence of TSD in fish and to furnish robust patterns of sex ratio response to temperature, we have used a comparative analysis consisting of the application of two independent criteria to identify the presence of TSD (Fig. 2). The first is that of Valenzuela et al. [2], which: (i) stresses that the presence of chromosomal systems of sex determination such as XX/XY or WZ/ZZ, that imply consistent genetic differences between sexes, constitutes a very strong evidence of the presence of GSD, and thus it is extremely unlikely that species with these chromosomal systems have TSD. The evidence for sex chromosomes may have been obtained with direct (karyotyping, banding) or indirect methods (e.g., progeny analysis of sex-linked traits, mating experiments or crosses with sex-reversed fish); (ii) considers induced sex ratio shifts that occur only at extreme (but not defined), ecologically irrelevant temperatures, not proof of TSD. The second criteria, which complements the former, is that of Conover [16], which establishes that in order for a species to have TSD, sex ratio shifts in response to temperature fluctuations must occur within a certain range, defined as the range of natural temperature (RNT) in which the species lives. However, since the thermosensitive period in the vast majority of fish examined so far is usually located during early development, and particularly during the larval stages [12]–[16], a modification of the criterion in Conover [16] was used for final assignment of TSD to a given species. Therefore, only those species for which sex ratio shifts occurred not within the RNT but instead within the RTD -the range of temperatures during the period of development that usually includes the thermosensitive period- were considered candidates for having TSD. Particularly in seasonally breeding species of temperate latitudes, RTD is contained within RNT but the opposite is not true (Table S1). Thus, response within the RNT is not enough evidence for TSD. Using the RTD instead of the RNT has the additional advantage of incorporating additional criteria of Valenzuela et al. [2] other than the absence of sex chromosomes, since it facilitates excluding cases of sex reversals induced at extreme temperatures, another possible source of confusion. When a species has a sex chromosomal system and/or sex ratio response to temperature occurring at extreme temperatures (sometimes close to the LT), and definitively outside the RTD (e.g., Fig. 3B), and hence ecologically irrelevant, then TSD is essentially very unlikely. These instances are more appropriately referred to as cases of naturally- or experimentally-induced alterations of genotypic sex determination or genotypic sex determination plus temperature effects (GSD+TE) [2], [16] rather than TSD. Thus, for any given species to have TSD, it should fulfill both of the following two conditions: 1) not having sex chromosomes, and 2) have sex ratio response to temperature within the RTD (Fig. 2). The possible error in proceeding in this manner is negligible and smaller than doing the opposite, i.e., classifying a species as having TSD that has sex chromosomes, which in most cases is strong evidence of GSD, and/or that exhibits sex ratio shifts at artificially high or low temperatures, which is ecologically irrelevant.


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

Ospina-Alvarez N, Piferrer F - PLoS ONE (2008)

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).
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2481392&req=5

pone-0002837-g003: 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).
Mentions: To determine the actual prevalence of TSD in fish and to furnish robust patterns of sex ratio response to temperature, we have used a comparative analysis consisting of the application of two independent criteria to identify the presence of TSD (Fig. 2). The first is that of Valenzuela et al. [2], which: (i) stresses that the presence of chromosomal systems of sex determination such as XX/XY or WZ/ZZ, that imply consistent genetic differences between sexes, constitutes a very strong evidence of the presence of GSD, and thus it is extremely unlikely that species with these chromosomal systems have TSD. The evidence for sex chromosomes may have been obtained with direct (karyotyping, banding) or indirect methods (e.g., progeny analysis of sex-linked traits, mating experiments or crosses with sex-reversed fish); (ii) considers induced sex ratio shifts that occur only at extreme (but not defined), ecologically irrelevant temperatures, not proof of TSD. The second criteria, which complements the former, is that of Conover [16], which establishes that in order for a species to have TSD, sex ratio shifts in response to temperature fluctuations must occur within a certain range, defined as the range of natural temperature (RNT) in which the species lives. However, since the thermosensitive period in the vast majority of fish examined so far is usually located during early development, and particularly during the larval stages [12]–[16], a modification of the criterion in Conover [16] was used for final assignment of TSD to a given species. Therefore, only those species for which sex ratio shifts occurred not within the RNT but instead within the RTD -the range of temperatures during the period of development that usually includes the thermosensitive period- were considered candidates for having TSD. Particularly in seasonally breeding species of temperate latitudes, RTD is contained within RNT but the opposite is not true (Table S1). Thus, response within the RNT is not enough evidence for TSD. Using the RTD instead of the RNT has the additional advantage of incorporating additional criteria of Valenzuela et al. [2] other than the absence of sex chromosomes, since it facilitates excluding cases of sex reversals induced at extreme temperatures, another possible source of confusion. When a species has a sex chromosomal system and/or sex ratio response to temperature occurring at extreme temperatures (sometimes close to the LT), and definitively outside the RTD (e.g., Fig. 3B), and hence ecologically irrelevant, then TSD is essentially very unlikely. These instances are more appropriately referred to as cases of naturally- or experimentally-induced alterations of genotypic sex determination or genotypic sex determination plus temperature effects (GSD+TE) [2], [16] rather than TSD. Thus, for any given species to have TSD, it should fulfill both of the following two conditions: 1) not having sex chromosomes, and 2) have sex ratio response to temperature within the RTD (Fig. 2). The possible error in proceeding in this manner is negligible and smaller than doing the opposite, i.e., classifying a species as having TSD that has sex chromosomes, which in most cases is strong evidence of GSD, and/or that exhibits sex ratio shifts at artificially high or low temperatures, which is ecologically irrelevant.

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Institut de Ciències del Mar, Consejo Superior de Investigaciones Científicas, Barcelona, Spain.

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.

Show MeSH
Related in: MedlinePlus