Evolution of sexuality: biology and behavior

Abstract

Sexual reproduction in animals and plants is far more prevalent than asexual reproduction, and there is no dearth of hypotheses attempting to explain why. Even bacteria and viruses, which reproduce by cloning, engage in promiscuous horizontal gene exchange ("parasexual reproduction") on such short time scales that they evolve genotypic diversity even more rapidly than eukaryotes. (We confront this daily in the form of antimicrobial resistance.) The host-parasite and host-pathogen arms race purports to explain the prevalence of sexual reproduction, yet there are over a dozen other hypotheses, including the proposition that sexual reproduction purges the genome of deleterious mutations. An equally daunting challenge is to understand, in terms of evolutionary logic, the jungle of diverse courtship and mating strategies that we find in nature. The phenotypic plasticity of sex determination in animals suggests that the central nervous system and reproductive tract may not reach the same endpoint on the continuum between our stereotypic male and female extremes. Why are there only two kinds of gametes in most eukaryotes? Why are most flowering plants, and few animals, hermaphroditic? Why do male animals compete more for access to females than the other way around in most animals that have been studied?This review presents more questions than answers, but an extraordinary wealth of data has been collected, and new genetic techniques will provide new answers. The possible relevance of these data to human sexuality will be discussed in a future article.

Figure 1

(a) Male Resplendent Quetzal in nest hole in Costa Rica, his long tail still pointing the way it did when he entered. The long tail and bright colors of many male birds are examples of female choice, a form of sexual selection, distinct from natural selection, even though it is still “natural.” The ornaments and colors of such male birds are actually survival handicaps, and research has shown that choice of such mates by females increases their reproductive success by providing them with robust genes and the likelihood that their male offspring will also be more attractive to females. (b) Female Resplendent Quetzal in Costa Rica, with a much shorter tail than the male and less bright colors.

Figure 2

Peacock with a highly ornamented tail which, like the male quetzal's tail, evolved by female choice. If some “eyes” are removed from his tail, he becomes less attractive to peahens. It is hard to imagine how such an enormous encumbrance would be compatible with escape from predators, and indeed further enlargement of the tail may have been constrained by natural selection.

Figure 3

Gary Larson got this one right!

Figure 4

Young male giraffes in East Africa gently spar for as long as an hour, in preparation for more serious sparring as adults in competition for females. The head and neck are also used as powerful weapons in killing predators.

Figure 5

Young male Australian sea lions confront each other in practice bouts of sparring, in preparation for competition for females as adults. Male-male competition is one form of sexual selection and often results in males being larger than females and having more formidable weaponry.

Figure 6

Adult male impalas clash in deadly earnest in competition for females and territory, in the Okavango Delta of Botswana, southern Africa.

Figure 7

Male elk with his harem in Yellowstone National Park. His antlers and larger size result from male-male competition, a form of sexual selection.

Figure 8

Lions mating in the Masai Mara of Kenya, with the male's grimace and female's reaction at the moment of ejaculation. The female mates with many males before “committing” her eggs to fertilization. When she accepts a male, they often copulate every 15 minutes for 3 days and nights, the male never letting her wander more than a few feet away. Infanticide by new males that take over a pride may help explain her delay in ovulating, as she may be testing the stability of her pride's male coalition.

Figure 9

A lioness licks her newborn cubs that were just delivered in a protected place away from the pride, probably for the safety of the cubs in the case of takeover by a new male coalition. Females tend to coordinate their pregnancies, and when their cubs are returned to the pride they are suckled by all lactating females. Lions are the only highly “social” cat; other cats around the world are solitary as adults, except for cheetah brothers, which may remain together.

Figure 10

“Pregnant” male seahorse, carrying his young in an abdominal pouch. His certainty of paternity is absolute, as the female injects her eggs into his pouch, where he fertilizes them. In some male seahorses there is a placenta-like structure for nourishing the young. His sperm count is low, as is predicted by evolutionary theory in the face of absent sperm competition with other males.

Figure 11

A female Argiope garden spider on her web in North Texas, with a zig-zag structure called the stabilimentum, the function of which is unknown. The male is a tiny fraction of her size, and after inserting his mating appendage into her genital aperture he dies spontaneously, of his own accord, remaining in place. One hypothesis is that he thus serves as a mating plug, a kind of chastity belt, temporarily blocking any other male from taking his turn.

Figure 12

Orange clownfish share a protective anemone on a Philippine coral reef. The female is largest and the male second largest. If the female dies, the male changes sex and takes her place, and the largest nonbreeder becomes the breeding male. Subordinates in the group queue for breeding positions.

Figure 13

This Wandering Albatross fledgling, on its nest on South Georgia Island, is almost ready to start an uninterrupted 5- to 7-year-long flight over the southern ocean surrounding the bottom of the world, returning to land after all those years to mate monogamously for life. Even at only 9 months of life, it has a wingspan of 11 feet, the longest of any bird; we were 20 feet away and it seemed like a giant.

Figure 14

Standing on his hands and rolling a ball of herbivore dung with his hind legs, a male dung beetle in East Africa courts a female in the process, who rides along on the ball. At some point he decides to start digging, and the party disappears slowly down the hole, to a depth of several feet. Once there the female deposits one or more eggs in the dung, now safe from predators. Dung beetles are unsung heroes of nutrient recycling and soil turnover in the tropics. We wear them on our body in the form of scarab jewelry.

Figure 15

The reproductive tract of the spotted hyena, an African carnivore, is unique in all the world and is outrageous in its risk factors. The fetus (shown) must pass through a tract which turns at almost 180 degrees and continues through the canal of the enlarged clitoris. The clitoris, a homolog of the penis, is enlarged in female spotted hyenas because of high androgen levels, thought to have evolved because they conferred survival benefits upon the female and her young by increasing her body size and dominance at highly competitive feeding opportunities at kills. The clitoris and penis look so much alike that experienced researchers have trouble distinguishing males from females, except by adult size. The vagina and urogenital canal of the female pass through the clitoris, as in no other known mammal. Obstructed labor and suffocation result in the death of a high percentage of neonates.

Figure 16

Naked mole-rats, which live underground in East Africa, are among the most unusual mammals in the world, almost hairless and almost blind, with only one reproductive female and several reproductive males. Other colony members specialize in colony tasks and do not reproduce; the caste system has been compared to eusocial insects, which also have nonproductive workers. This small group of nonreproductive workers was collected by a researcher in East Africa whom we encountered on a dirt road, where he was capturing workers that appeared at the surface while excavating cavity tunnels. They are caught by snakes in the same way, as they emerge at the surface. A colony may comprise 80 individuals, or sometimes up to several hundred, and feed on plant roots and tubers underground. This diet is high in cellulose, which is difficult to digest. Their gut microbiota help with digestion, and coprophagy (ingestion of feces) allows maximal extraction of nutrients.

Figure 17

Golden toads, this pair in amplexus in the cloud forest of Monteverde, Costa Rica, have never been seen since 1989. The small and isolated populations, which occupied only a few square mi les of cloud forest, are now apparently extinct, and their social behavior has never been studied in detail. Many biologists have searched for them in vain. At large pools of rainwater in the rainy season, as many as several hundred males were once seen at one time; for the lucky few who saw them, the sight was unforgettable.