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Authors: David P. Barash

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An especially intriguing evolutionary principle is known as the Red Queen Effect, after the scene in Lewis Carroll’s
Through the Looking Glass
, in which the Red Queen grabs Alice’s hand and insists that they run. It soon becomes apparent, however, that they aren’t getting anywhere:

“Well, in our country,” said Alice, still panting a little, “you’d generally get to somewhere else—if you run very fast for a long time, as we’ve been doing.”

 

“A slow sort of country!” said the Queen. “Now, here, you see, it takes all the running you can do, to keep in the same place. If you want to get somewhere else, you must run at least twice as fast as that!”

 

Biologists seized upon this image to describe the need of organisms to be constantly evolving so as to keep up with changes in their ecological niche. It could well be that the Red Queen Effect is particularly active with regard to the evolution of sex itself, with our understanding of ecological niche expanded to include not just the “outside” environment, but also the various pathogens and parasites residing inside everyone’s body. As primatologist Allison Jolly pointed out in a delightful limerick, this gives new meaning to the expression “keeping up with the Joneses”:

Your kids must keep up with the Joneses;

 

relaxation’s forever denied you.

 

For the reasons you’ve kids and not clones is,

 

the Joneses are living inside you
31

 

A research report titled “Running with the Red Queen: Host-Parasite Coevolution Selects for Biparental Sex” provided evidence for just this sort of competition between free-living organisms and their internal, parasitic “Joneses.” The biologists took a species of nematode worm that can reproduce sexually as well as asexually and infected it with some nasty bacteria that digest their “hosts” from the inside out. Two different populations were compared: one infected with the bacteria and another that wasn’t. Over time, the infected population of worms evolved to engage in significantly more sexual reproduction. In addition, obligately
asexual populations infected with the bacteria went extinct quite rapidly, whereas those that were capable of sexual reproduction persisted over time, presumably because they were able to remain at least one genetic step ahead of their lethal fellow travellers.
32

N
ext, we turn to yet another human sexual mystery, one that is limited to a minority of the population but that is nonetheless among the most perplexing of all.

Notes
 

1
. Fox, C. A., Wolff, H. S., & Baker, J. A. (1970). Measurement of intra-vaginal and intra-uterine pressures during human coitus by radio-telemetry.
Journal of Reproduction and Fertility, 22,
243–251.

2
. Baker, R. R., & Bellis, M. A. (1993). Human sperm competition: Ejaculate manipulation by females and a function for the female orgasm.
Animal Behaviour, 46,
887–909.

3
. Shklovsky, V. (2005).
Knight’s move
. Champaign, IL: Dalkey Archive Press.

4
. Symons, D. (1979).
The evolution of human sexuality
. New York: Oxford University Press.

5
. Gould, S. J. (1987). Freudian slip.
Natural History, 96,
14–21.

6
. Lloyd, E. (2005).
The case of the female orgasm
. Cambridge, MA: Harvard University Press.

7
. Dunn K. M., Cherkas, L. F., & Spector, T. D. (2005). Genetic influences on variation in female orgasmic function: A twin study.
Biology Letters, 1,
260–263; Dawood, K., Kirk, K. M., Bailey, J. M., Andrews, P. W., & Martin, N. G. (2005). Genetic and environmental influences on the frequency of orgasm in women.
Twin Research and Human Genetics, 8
(1), 27–33.

8
. Connell, K., Guess, M. K., La Combe, J., Wang, A., Powers, K., Lazarou, G., et al. (2005). Evaluation of the role of pudendal nerve integrity in female function using noninvasive techniques.
American Journal of Obstetrics and Gynecology, 192
(5), 1712–1717.

9
. Hrdy, S. B. (1979). Infanticide among animals: A review, classification, and examination of the implications for the reproductive strategies of females.
Ethology and Sociobiology, 1,
13–40.

10
. Hrdy, S. B. (2000).
Mother nature
. New York: Ballantine Books.

11
. Komisaruk, B. R., Beyer-Flores, C., & Whipple, B. (2006).
The science of orgasm.
Baltimore: Johns Hopkins University Press.

12
. Nin, A. (1970).
The diary of Anaïs Nin
(Vol. 2). New York: Harcourt, Brace, Jovanovich.

13
. Troisi, A., & Carosi, M. (1998). Female orgasm rate increases with male dominance in Japanese macaques.
Animal Behaviour, 56,
1261–1266.

14
. Eschler, L. (2004). The physiology of the female orgasm as a proximate mechanism.
Sexualities, Evolution and Gender, 6,
171–194.

15
. Kiefer, A. K., Sanchez, D. T., Kalinka, C. J., & Ybarra, O. (2006). Sex roles how women’s nonconscious association of sex with submission relates to their subjective sexual arousability and ability to reach orgasm.
55,
83–94.

16
. March of Dimes. Retrieved from
http://www.marchofdimes.com/professionals/681_1155.asp
.

17
. Marlowe, F. (2000). The Patriarch Hypothesis: An alternative explanation of menopause.
Human Nature, 11,
27–42.

18
. The Jane Goodall Institute. Retrieved from
http://www.janegoodall.org/chimp_central/chimpanzees/f_family/flo.asp
.

19
. Hrdy, S. B. (2005). Cooperative breeders with an ace in the hole. In: E. Voland, A. Chasiotis, & W. Schiefenhoevel (Eds.),
Grandmotherhood: The evolutionary significance of the second half of female life
(pp. 295–317). New Brunswick, NJ: Rutgers University Press.

20
. Hawkes, K., O’Connell, J. F., & Blurton Jones, N. G. (1997). Hadza women’s time allocation, offspring provisioning and the evolution of long postmenopausal life spans.
Current Anthropology, 38,
551–578.

21
. For example, Sear, R., Mace, R., & McGregor, I. A. (2000). Maternal grandmothers improve the nutritional status and survival of children in rural Gambia.
Proceedings of the Royal Society of London, B, 267,
1641–1647.

22
. Cant, M. A., & Johnstone, R. A. (2008). Reproductive skew and the evolution of menopause. In: R. Hagar & C. B. Jones (Eds.),
Reproductive skew in vertebrates
. Cambridge, UK: Cambridge University Press.

23
. Dawkins, R. (1989).
The selfish gene
. New York: Oxford University Press.

24
. Hrdy, S. B. (1999).
Mother nature: Maternal instincts and how they shape the human species
. New York: Ballantine.

25
. Saad, G. (2004). Applying evolutionary psychology in understanding the representation of women in advertisements.
Psychology and Marketing, 21,
593–612.

26
. Gwynne, D. T. (1981). Sexual different theory: Mormon crickets show role reversal in mate choice.
Science, 213,
779–780.

27
. Hamilton, J. B., & Mestler, G. E. (1969). Mortality and survival: comparison of eunuchs with intact men and women in a mentally retarded population.
Journal of Gerontology, 24,
395–411.

28
. Dingard, D. L. (1984). The sex differential in morbidity, mortality and lifestyle.
Annual Review of Public Health, 5,
433–458.

29
. Williams, G. C. (1957). Pleiotropy, natural selection, and the evolution of senescence.
Evolution, 11,
398–411.

30
. Williams, G. C. (1975).
Sex and evolution.
Princeton, NJ: Princeton University Press.

31
. Jolly, A. (2000).
Lucy’s legacy: Sex and intelligence in human evolution.
Cambridge, MA: Harvard University Press.

32
. Morran, L. T., Schmidt, O. G., Gelarden, I. A., Parrish II, R. C., & Lively, C. M. (2011). Running with the Red Queen: Host-parasite coevolution selects for biparental sex.
Science, 333,
216–218.

C
HAPTER
F
OUR
Sexual Mysteries III:
Homosexuality

H
OMOSEXUALITY
, “
THE LOVE THAT
dares not speak its name,” speaks loudly indeed when it comes to posing an evolutionary mystery. The mystery is simple enough; its resolution, however, is not yet in sight. First, the mystery.

 
Partitioning the Puzzle
 

The
sine qua non
for any trait to have evolved is for it to connect positively with reproductive success, more precisely, with success in projecting genes relevant to that trait into the future. So, if homosexuality is in any sense a product of evolution—and it clearly is, for reasons to be explained—then genetic factors associated with same-sex preference must enjoy “positive selection pressure,” which is to say, some sort of fitness advantage. The problem should be obvious: How can natural selection have favored any genes whose phenotypic outcome (anatomy, physiology, or behavioral inclination) results in its own diminished success? By definition, they should be selected against. And pretty much by definition, homosexuals should experience less reproductive success than
their heterosexual colleagues. Yet, as we’ll see, same-sex preference clearly has a genetic component, which is to say, it must have evolved. But how?

 

The paradox of homosexuality is especially apparent for individuals whose homosexual preference is exclusive; that is, who have no inclination toward heterosexuality. But the paradox persists even for those who are bisexual, since it is mathematically provable that even a tiny difference in reproductive outcome can drive substantial evolutionary change. One of the giants of evolutionary theory, J. B. S. Haldane, made the following calculation in 1927 (it loomed large in the about-to-emerge “synthetic theory of evolution,” which crucially combined genetics and natural selection).

Haldane suggested that we imagine two alternative forms of the same gene—that is, two “alleles”—call them A1 and A2.
i
Lets say that the initial frequency of A1 is 0.1% and that of A2 is 99.9%. Imagine, further, that A1 produces 101 successful offspring for every 100 produced by A2; that is, A1 enjoys a very slight fitness advantage of just 1%. Despite the fact that it starts off being so rare that its numbers seem downright insignificant (merely one A1 allele for every 1,000 A2s), and despite the fact that it does only 1% better than its rival, in just 4,000 generations the situation would have reversed, with A1 now making up 99.9% of the population and A2, a mere .1%.
1
Such is the power of compound interest, and of natural selection.

For our purposes, the implication is dramatic: Anything that diminishes, even slightly, the reproductive performance of a given allele should be vigorously selected against. And homosexuality certainly seems like one of these things. Gay men, for example, have children at about 20% the rate of heterosexual men.
2
I haven’t
seen reliable data for lesbians, but it seems highly likely that a similar pattern exists.

Of course, many homosexuals are actually bisexual, and as a result, they reproduce heterosexually, at least some of the time. True enough. In fact, Alfred Kinsey and his collaborators developed a useful 7-point scale concerning human sexual preferences, ranging from exclusive heterosexuality to exclusive homosexuality. They emphasized that when it came to human beings, same-sex and opposite-sex preferences do not constitute two distinct and nonoverlapping populations. “The world,” Kinsey et al. pointed out, “is not divided into sheep and goats.”
3

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