Environmental and Chromosomal Sex Determination

In the course of evolution, some processes move easily from environmental control to genetic control and back again. It may seem odd to think of sex determination as a response to the environment, but it is one of the clearest examples of the interchangeability of physiological and genetic control. In many organisms, fish and reptiles included, the ratio of males to females may deviate far from unity depending on environmental conditions such as temperature or social interactions. Summarizing the knowledge in 1900, E. B. Wilson (later, ironically, one of the discoverers of sex chromosomes) wrote: "Sex as such is not inherited. What is inherited is the capacity to develop into either male or female, the actual result being determined by the combined effect of conditions external to the primordial germ-cell." The discovery in 1905 of the genetic basis of sex is considered one of the great triumphs of early-twentieth-century biology. Nettie Stevens of Bryn Mawr College provided convincing evidence for the control of sex by the balance of X and Y chromosomes, based on her studies in over 50 species of beetles. She found that females always possessed two X chromosomes; males usually had one X and a smaller Y chromosome, although some species lacked a Y altogether. She and Wilson independently published monumental papers concluding that chromosomes determine sex. As we noted in Chapter 1, T. H. Morgan's first great achievement in genetics was his analysis of a white-eyed male, where eye color was linked to maleness. It gave incontrovertible functional proof in fruit flies (later in many other animals) that females carried two copies of the X chromosome, whereas males carried one. In contrast, organisms with environmental sex determination showed no chromosome difference between males and females.14

It is surprising that the mechanism for sex determination is not as universal as the processes of meiosis and fertilization on which sexual reproduction depends. In crocodiles and many species of lizards and turtles, sex is determined in an extremely narrow range by the ambient temperature at which the egg develops. For example, American alligator eggs incubated at 86° F (30o C) produce 100 percent females, whereas at 91° F (33° C) they produce 100 percent males. The embryonic animals are sensitive to temperature during a particular week of their nine-week period of development, as the sex organs begin to take on characteristics of either the testis or the ovary. Before this time, the developing sex organs look the same in all individuals and can become either testis or ovary. The organ is called the indifferent gonad at this stage. At 910 F (330 C) in the critical week, large cells proliferate and surround the germ cells. They will form the Sertoli cells, which play a critical role in the development of the testis and spermatozoa; a male results. At 860 F (30O C) in the critical week, the germ cells proliferate and form clusters. The large cells fail to proliferate and disappear; an ovary develops and a female results, as illustrated in Figure 14.15

What is the temperature-dependent step of sex determination of reptiles, recognizing of course that the early development of the gonad is the same in both sexes and is temperature independent? And what has replaced the temperature-dependent step (if that is the right way of thinking about it) in mammals and birds, all of which have chromosomal sex determination? How could testis and ovary development look initially so similar in mammals and reptiles, and at the same time be under such different controls?

The key to understanding the physiology is a circuit with two stable states (male and female), a circuit that can flip-flop between the two. At intermediate temperatures, intermediate proportions of males and females are produced, not intersexes or hermaphrodites. One clue is that in the critical period of development, alligator eggs at the temperature normally producing males can be entirely switched to females by exposing them to estradiol, the female sex hormone. Similarly, under conditions where females are normally produced, chemically inhibiting estradiol synthesis leads to the development entirely of males.

One may infer that if estradiol production were itself temperature sensitive, it could serve as the trigger for environmentally controlled sex determination. Carefully poised switches would be easy to control genetically as well as environmentally and could bring an entire suite of activities under the control of mutation, facilitating rapid evolutionary changes. To appreciate how switches could be thrown both genetically and environmentally, we need a molecular description of the process.

Universal Veil Mushroom Diagram

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