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Gilbert SF. Developmental Biology. 6th edition. Sunderland (MA): Sinauer Associates; 2000.

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Developmental Biology. 6th edition.

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Environmental Sex Determination

Temperature-dependent sex determination in reptiles

While the sex of most snakes and most lizards is determined by sex chromosomes at the time of fertilization, the sex of most turtles and all species of crocodilians is determined by the environment after fertilization. In these reptiles, the temperature of the eggs during a certain period of development is the deciding factor in determining sex, and small changes in temperature can cause dramatic changes in the sex ratio (Bull 1980). Often, eggs incubated at low temperatures (22–27°C) produce one sex, whereas eggs incubated at higher temperatures (30°C and above) produce the other. There is only a small range of temperatures that permits both males and females to hatch from the same brood of eggs. Figure 17.20 shows the abrupt temperature-induced change in sex ratios for the red-eared slider turtle. If eggs are incubated below 28°C, all the turtles hatching from them will be male. Above 31°C, every egg gives rise to a female. At temperatures in between, the broods will give rise to individuals of both sexes. Variations on this theme also exist. The eggs of the snapping turtle Macroclemys, for instance, become female at either cool (22°C or lower) or hot (28°C or above) temperatures. Between these extremes, males predominate.

Figure 17.20. Temperature-dependent sex determination in three reptile species: the American alligator (Alligator mississippiensis), the red-eared slider turtle (Trachemys scripta elegans), and the alligator snapping turtle (Macroclemys temminckii).

Figure 17.20

Temperature-dependent sex determination in three reptile species: the American alligator (Alligator mississippiensis), the red-eared slider turtle (Trachemys scripta elegans), and the alligator snapping turtle (Macroclemys temminckii). (After Crain and (more...)

One of the best-studied reptiles is the European pond turtle, Emys obicularis. In laboratory studies, incubating Emys eggs at temperatures above 30°C produces all females, while temperatures below 25°C produce all-male broods. The threshold temperature (at which the sex ratio is even) is 28.5°C (Pieau et al. 1994). The developmental period during which sex determination occurs can be discovered by incubating eggs at the male-producing temperature for a certain amount of time and then shifting the eggs to an incubator at the female-producing temperature (and vice versa). In Emys, the last third of development appears to be the most critical for sex determination. It is not thought that turtles can reverse their sex after this period.

The pathways toward maleness and femaleness in reptiles are just being delineated. Unlike the situation in mammals, sex determination in reptiles (and birds) is hormone-dependent. In birds and reptiles, estrogen is essential for ovarian development. Estrogen can override temperature and induce ovarian differentiation even at masculinizing temperatures. Similarly, injecting eggs with inhibitors of estrogen synthesis will produce male offspring, even if the eggs are incubated at temperatures that usually produce females (Dorizzi et al. 1994; Rhen and Lang 1994). Moreover, the sensitive time for the effects of estrogens and their inhibitors coincides with the time when sex determination usually occurs (Bull et al. 1988; Gutzke and Chymiy 1988).

It appears that the enzyme aromatase (which can convert testosterone into estrogen) is important in temperaturedependent sex determination. The estrogen synthesis inhibitors used in the experiments mentioned above worked by blocking the aromatase enzyme, showing that experimentally low aromatase conditions yield male offspring. This correlation is seen to hold under natural conditions as well. The aromatase activity of Emys is very low at the male-promoting temperature of 25°C. At the female-promoting temperature of 30°C, aromatase activity increases dramatically during the critical period for sex determination (Desvages et al. 1993; Pieau et al. 1994). Temperature-dependent aromatase activity is also seen in diamondback terrapins, and its inhibition masculinizes their gonads (Jeyasuria et al. 1994). One remarkable finding is that the injection of an aromatase inhibitor into the eggs of an all-female parthenogenetic species of lizards causes the formation of males (Wibbels and Crews 1994).

It is not known whether the temperature sensitivity resides in the aromatase gene or protein itself or in other proteins that regulate it. One hypothesis is that the temperature is sensed by neurons in the central nervous system and transduced to the bipotential gonad by nerve fibers (see Lance 1997). Another hypothesis is that aromatase activity may be regulated by Sox9. This sex-determining gene is seen throughout the vertebrates, where its expression in gonads correlates extremely well with the production of testes. When two species of turtles were raised at female-promoting temperatures, Sox9 expression was down-regulated during the critical time for sex determination. However, in the bipotential gonads of those turtles raised at male-promoting temperatures, Sox9 expression was retained in the medullary sex cords destined to become Sertoli cells (Spotila et al. 1998; Moreno-Mendoza et al. 1999).

The evolutionary advantages and disadvantages of temperature-dependent sex determination are discussed in Chapter 21. Recent studies (Bergeron et al. 1994, 1999) have shown that polychlorinated biphenyl compounds (PCBs), a class of widespread pollutants that can act like estrogens, are able to reverse the sex of turtles raised at “male” temperatures. This knowledge may have important consequences in environmental conservation efforts to protect endangered turtle species.

Location-dependent sex determination in Bonellia and Crepidula

As mentioned in Chapter 3, the sex of the echiuroid worm Bonellia depends on where a larva settles. If a Bonellia larva lands on the ocean floor, it develops into a 10-cm-long female. If the larva is attracted to a female's proboscis, it travels along the tube until it enters the female's body. Therein it differentiates into a minute (1–3-mm-long) male that is essentially a sperm-producing symbiont of the female (see Figure 3.1).

Another example in which sex determination is affected by the location of the organism is the case of the slipper snail Crepidula fornicata. In this species, individuals pile up on top of one another to form a mound (Figure 17.21). Young individuals are always male. This phase is followed by the degeneration of the male reproductive system and a period of lability. The next phase can be either male or female, depending on the animal's position in the mound. If the snail is attached to a female, it will become male. If such a snail is removed from its attachment, it will become female. Similarly, the presence of large numbers of males will cause some of the males to become females. However, once an individual becomes female, it will not revert to being male (Coe 1936). More examples of context-dependent sex determination will be studied in Chapter 21.

Figure 17.21. Cluster of Crepidula snails.

Figure 17.21

Cluster of Crepidula snails. Two individuals are changing from male to female. After these molluscs become female, they will be fertilized by the male above them. (After Coe 1936.)

Nature has provided many variations on her masterpiece. In some species, including most mammals and insects, sex is determined solely by chromosomes; in other species, sex is a matter of environmental conditions. We are finally beginning to understand the mechanisms by which this masterpiece is created.

By agreement with the publisher, this book is accessible by the search feature, but cannot be browsed.

Copyright © 2000, Sinauer Associates.
Bookshelf ID: NBK9989

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