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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 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.
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pone-0002837-g001: 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.

Mentions: In fish, the first evidence of TSD was obtained in field and laboratory studies carried out in the Atlantic silverside, Menidia menidia (F. Atherinopsidae) [11]. Since then, TSD has been claimed in 59 different species (33 of them of the genus Apistogramma, F. Cichlidae, and all included in the same study) belonging to 13 families representative of many types of fishes (see Table S1 in the Supplementary Materials). Fish with TSD have readily been grouped according to three patterns of sex ratio response to environmental temperature [12]–[16]: 1, more males at high temperature; 2, more males at low temperature; and 3 more males at extreme (high and low) temperatures (Fig. 1). However, a critical examination of sex ratio produced in response to temperature in fish has never been carried out. Based on all the available data on TSD in fish, it has been reported that 53–55 (including the 33 species of the genus Apistogramma), 2–4 and 2 of these species follow patterns 1, 2 and 3, respectively (Table 1). Note that what here are referred to as patterns 1 and 2 of fish essentially corresponds to what in reptiles are referred to as patterns Ib and Ia, respectively. However, pattern 3 of fish is not equivalent to pattern II of reptiles (female-biased sex ratios at low and high temperatures and male-biased sex ratios at intermediate temperatures) but it could be considered an inverse of it.


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 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.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2481392&req=5

pone-0002837-g001: 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.
Mentions: In fish, the first evidence of TSD was obtained in field and laboratory studies carried out in the Atlantic silverside, Menidia menidia (F. Atherinopsidae) [11]. Since then, TSD has been claimed in 59 different species (33 of them of the genus Apistogramma, F. Cichlidae, and all included in the same study) belonging to 13 families representative of many types of fishes (see Table S1 in the Supplementary Materials). Fish with TSD have readily been grouped according to three patterns of sex ratio response to environmental temperature [12]–[16]: 1, more males at high temperature; 2, more males at low temperature; and 3 more males at extreme (high and low) temperatures (Fig. 1). However, a critical examination of sex ratio produced in response to temperature in fish has never been carried out. Based on all the available data on TSD in fish, it has been reported that 53–55 (including the 33 species of the genus Apistogramma), 2–4 and 2 of these species follow patterns 1, 2 and 3, respectively (Table 1). Note that what here are referred to as patterns 1 and 2 of fish essentially corresponds to what in reptiles are referred to as patterns Ib and Ia, respectively. However, pattern 3 of fish is not equivalent to pattern II of reptiles (female-biased sex ratios at low and high temperatures and male-biased sex ratios at intermediate temperatures) but it could be considered an inverse of it.

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