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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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Related in: MedlinePlus

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.
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pone-0002837-g004: 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.

Mentions: Our results show that of the 53–55 species (depending on the authors) previously assigned to pattern 1, the 33 cichlid species of the genus Apistogramma indeed exhibit pattern 1 (Fig. 3A a; Table 1) fulfilling the criteria for the assignment of TSD. However, only seven other species of the remaining 20–22 adhere to pattern 1 and have TSD (Fig. 3A b,c). In all but one of the species with TSD the best fit to the experimental data on sex ratio response to temperature was obtained with a linear regression (Y = a+bX). In Menidia menidia, however, the best fit was obtained with a reciprocal-X model (Y = a+b/X) (Fig. 4). Included among the species that did not pass the criteria to be diagnosed as true cases of TSD are some established research models such as the zebrafish (Danio rerio) and the medaka (Oryzias latipes) (Fig. 3B a,b).


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 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.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2481392&req=5

pone-0002837-g004: 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.
Mentions: Our results show that of the 53–55 species (depending on the authors) previously assigned to pattern 1, the 33 cichlid species of the genus Apistogramma indeed exhibit pattern 1 (Fig. 3A a; Table 1) fulfilling the criteria for the assignment of TSD. However, only seven other species of the remaining 20–22 adhere to pattern 1 and have TSD (Fig. 3A b,c). In all but one of the species with TSD the best fit to the experimental data on sex ratio response to temperature was obtained with a linear regression (Y = a+bX). In Menidia menidia, however, the best fit was obtained with a reciprocal-X model (Y = a+b/X) (Fig. 4). Included among the species that did not pass the criteria to be diagnosed as true cases of TSD are some established research models such as the zebrafish (Danio rerio) and the medaka (Oryzias latipes) (Fig. 3B a,b).

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