Biological Exuberance: Animal Homosexuality and Natural Diversity

instance, are not “prevented” from mating by older males—they simply do not participate to the same extent (as discussed in chapter 4). In other species—particularly birds with communal breeding systems such as the Pied Kingfisher, as well as primates such as tamarins and marmosets—scientists describe individuals not as “unwillingly” suppressed in their reproductive efforts, but rather as “choosing” to forgo reproduction or exercising “self-restraint” in their reproductive participation.⁹⁴ Further evidence that animals are often “voluntary” nonbreeders involves species such as Ocher-bellied Flycatchers and Ruffed Grouse, where prime breeding territories often go unused even though many nonreproducing individuals are in the population. Sometimes physiological mechanisms are involved in nonbreeding, such as lowered hormonal levels, delay of sexual maturation (sometimes indefinitely), inhibition of ovulation, and even blocking of pregnancy following conception (seen in many rodents).⁹⁵

Finally, reproduction is often a physically demanding and exceedingly dangerous undertaking that some animals may simply “avoid.” Nonbreeders are often in better physical condition than breeders, since they do not have to experience the rigors of reproducing and parenting. In fact, breeding could even be considered “suicidal” in some cases, since it may lead to a reduced life expectancy. Male Bighorn Sheep and female Red Deer that breed, for example, have significantly higher mortality rates than nonbreeders. In several species of carnivorous marsupials, most males die after mating while nonbreeders generally survive longer. The life expectancy of nonbreeding male Ruffed Grouse often exceeds that of breeding males. And female Western Gulls that breed more often during their lives have a lower survival rate than individuals that are less reproductively “prolific.” Sometimes specific biological factors serve to discourage breeding, such as the astonishing phenomenon of clitoral, as opposed to vaginal, births in the Spotted Hyena. Many females of this species die during their first pregnancy or labor because their genital anatomy requires the baby to be born through the clitoris, which ruptures and often results in many other complications for both mother and fetus.⁹⁶ Finally, the risk of acquiring sexually transmitted diseases (which are found in a surprising number of animals) may also affect reproductive activity. For example, female Razorbills (a kind of bird) avoid reproductive copulations with males when the risk for infection from STDs is greatest (although they continue to have nonprocreative sex, i.e., mounting without direct genital contact). Heterosexual behavior in a number of other species may also be curtailed by the potential danger of STDs.⁹⁷

In the end, then, there is no single “reason” why animals don’t reproduce: nonbreeding, like sexuality, is simply a part of the fabric of animals’ lives, manifesting itself in many different ways. Heterosexuality constitutes a whole range of behaviors and life histories, not a single, inalterable template that every animal must follow. And nonbreeding is one of the many ways to be “heterosexual.” Regardless of the number of nonprocreating animals in a particular population or the “causes” of their nonbreeding, one thing is certain: nonreproducing (heterosexual) animals are a ubiquitous feature of animal life.

Worlds Apart: Sex Segregation, Hostility, and the Dark Side of Heterosexuality

Adult males and females [of the Sperm Whale] have lifestyles so distinct that they might be separate species. The males leave tropical waters each summer and voyage into the highest latitudes … but females and young seldom venture more than 40° from the equator.

—LYALL WATSON, Sea Guide to Whales of the World⁹⁸

Heterosexual mating is anything but the “natural,” effortless activity that it is often portrayed as. There are many ways that sexual interactions between males and females are avoided, exacerbated, or generally fraught with problems. In numerous animals, for example, it almost seems that the social organization and behaviors of the species have been designed to keep males and females apart and prevent reproduction —or at least make it difficult. Consider sex segregation: partial or total separation of males and females is a surprisingly prevalent form of social organization in the animal world. Various forms of sex segregation occur in mammals and birds of all types, though separation of the sexes is especially prevalent in species such as hoofed mammals that have promiscuous or polygamous mating systems (where individuals mate with more than one partner). Often the only time that the two sexes come together is to mate, sometimes for only a few days or months out of the year—the rest of their time is spent living entirely apart. Even “harems”—in which one male associates with a group of females and often prevents other males from gaining access to them—are not the quintessential example of heterosexual mating opportunity that they are usually thought to be. Scientists studying “harems” in a number of species such as sea lions and some hoofed mammals have found that these groups do not always form as a result of heterosexual attraction or males “controlling” females (and thus the term is somewhat inaccurate). Rather, females prefer to associate with each other and therefore they congregate in relatively autonomous groups of their own; males that participate in breeding then end up associating with such groups out of necessity.⁹⁹ In addition to social and spatial segregation—living in separate groups or habitats—sex segregation can also be seasonal or migratory. It may occur only during the nonbreeding season, for example, or involve separate migratory journeys or latitudinal destinations for males and females (for example, in Northern Elephant Seals and Kestrels). One of the most extreme forms of “sex segregation” occurs in several species of marsupial mice: all the males die a few days after the mating season, so that when females give birth there are no adult males left in the population.¹⁰⁰

Sex segregation during the breeding season is often facilitated by a phenomenon known as sperm storage: most female animals have one or more special organs or sites in their reproductive tract that allow them to store a cache of sperm (from a prior mating) for a long time, using it later to “inseminate” themselves while forgoing heterosexual copulations. Birds and reptiles have special glands that allow them to do this. Female Ruffs, for example, often leave the breeding grounds (after having mated with males) and migrate northward, laying their eggs several weeks later by fertilizing them with stored sperm. In some birds such as the fulmar, sperm may be stored by females for up to eight weeks, while in reptiles (as well as insects) sperm stored in females may remain viable for much longer, up to several months or even years. Female garter snakes, for instance, are able to keep sperm for up to three to six months after mating with a male. In fact, females in this species usually do not ovulate until two to five weeks after their first mating in the spring. They may even become pregnant without mating at all that season, simply by using sperm from a copulation that took place the previous fall before hibernation. The record for sperm storage is held by the female Javan wart snake, who can store sperm for up to seven years! In mammals, sperm is generally “stored” for shorter periods (although some bats can do so for more than six months) and may be kept in “crypts” on the cervix or inside the uterus. Recent work has also shown that females in most species can control, through behavioral, anatomical, and physiological mechanisms, which portion of the sperm (if any) is stored and/or utilized for fertilization.¹⁰¹

A phenomenon known as delayed implantation also enables males and females to spend long periods away from each other. In nearly 50 mammalian species (including seals, bears, other carnivores, marsupials, and some bats) the fertilized egg does not implant right away. It remains in “suspended animation” for several months, after which it implants and begins its regular development. The delay extends the pregnancy by two to five months in seals and up to ten to eleven months in badgers, fishers, stoats, and related small carnivores. In seals, this allows females to spend a longer time out at sea—often completely separate from males—and permits them to optimize the timing of their pregnancies and to take advantage of more favorable times of the year for birthing and pup- raising. Some species of bats also have delayed embryonic development, in which the fertilized egg experiences a temporary cessation of development after implantation.¹⁰²

In fact, delayed implantation as well as sperm storage (among a variety of other factors) effectively result in a separation and reordering of key reproductive events in many vertebrates, and consequently an “uncoupling” of male and female reproductive cycles. We are used to thinking of breeding as an ordered progression, one stage leading inevitably to the next: ovulation followed by mating followed by fertilization followed by pregnancy followed by birth (or egg laying). However, there are often significant gaps and rearrangements of these events: sperm storage can temporally separate mating from fertilization, while delayed implantation separates fertilization from fetal development during pregnancy. As noted above, sperm storage can also result in ovulation taking place after insemination, and in other animals, further rearrangements occur. In birds, for example, “pregnancy” or the development of the egg inside the mother’s body actually precedes fertilization: the egg yolks are already quite large (and may cause a noticeable bulge and weight increase in the female) prior to being fertilized. In fact, the eggs can be laid without ever being fertilized—this is what allows females in homosexual pairs to produce (infertile) eggs. In most fishes, “pregnancy” ends, rather