Repro Duction in Monkeys, Apes, and H[Umanrler B13eilnlges

Sexual Selection and the Comparative Anatomy of Repro duction in Monkeys, Apes, and H[umanRLER B13eiLnLges Alan Dixson and Matthew Anderson Center for Reproduction of Endangered Species Zoological Society of San Diego Sexual selection has had profound effects at the copulatory and postcopula- tory levels, upon the evolution of reproductive anatomy, physiology, and patterns of mating behavior. This review deals with the effects of sexual selection upon the evolution of relative testes sizes, sperm morphology, semi- nal vesicular function, penile morphology, and copulatory behavior in the Order Primates. The concept of cryptic female choice is also discussed, and its potential value in understanding how co-evolution of genital morphologies may have occurred in primates and in other animals. Key Words: cryptic female choice, genitalia, primates, sexual behavior, sexual selection, sperm competition. During the last 30 years, research on the evolution of reproduction has been revitalized by Parker's theory of 'sperm competition" (Parker, 1970) and by Eberhard's contributions to understanding genitalic evolution (Eberhard, 1985, 1996). The classical Darwinian view of precopula- toryz sexual selection (Andersson, 1994; Darwin, 1871) has expanded to embrace the realization that sexual selection also operates during and after copulation to influence the evolution of reproductive anatomy, physiology, and patterns of sexual behavior. Much of this newer research has involved insects and other invertebrates. However, these advances have had wide-ranging implications for understanding the evolution of reproduction in the vertebrates, including the primates (Birkhead & M0ller, 1992, 1998; Dixson, 1998a, Smith, 1984). The pur- pose of the present paper is to review advances in sexual selection theory as they apply specifically to our understanding of sperm competition, genitalic evolution, and copulatory behavior in monkeys, apes, and human beings. Correspondence concerning this article should be addressed to Alan Dixson, Center for Reproduction of Endangered Species, Zoological Society of San Diego, Post Office Box 120551, San Diego, CA 92112-0551. ([email protected]) 121 122 A. DIXSON & M. ANDERSON Sperm Competition and Cryptic Female Choice Parker originally defined sperm competition as "competition within a single female between the sperm of two or more males for the fertilization of the ova" (Parker, 1970, p. 527). More recently he has modified this definition to include species that employ external fertilization, so that sperm competition involves "competition between the sperm of two or more males for the fertilization of a given set of ova" (Parker, 1998, p. 4). For the primates, as for all mammals, his original definition holds because sperm competition occurs within the female's reproductive tract. However, the female's reproductive system is not necessarily a passive arena for competition between the ejaculates of rival males. Anatomical and physiological sieves and barriers within the vagina, cervix, uterus, uterotubal junction, and oviduct are all potential "hurdles" that might bias the outcome of sperm competition. In recognition of these possibilities, William Eberhard has used the term cryptic female choice to denote the possibility that sexual selection may involve hidden female effects upon the success of males in fertilizing ova (Eberhard, 1985, 1996). If we consider, for example, a female chimpanzee mating with several partners in rapid succession, as happens in nature (Goodall, 1986), then sperm competition is likely to occur. However, if one male possesses a more advantageous phallic morphology, or copulatory pattern, or a more biochemically efficient mixture of accessory sexual secretions, then the female's tract may preferentially receive and transport his spermatozoa, providing him with an advantage in the competitive process. It is this "hidden" potential which Eberhard refers to as cryptic female choice. It may explain, for example, why sexual selection has favored the evolution of complex phallic morphologies in many species in which females mate with multiple males. The phallus may function as "an internal courtship device" under such conditions (Eberhard, 1985). The terminology suggested by Eberhard seems prefer- able to the alternative of "female sperm choice" proposed, for example, by Birkhead (1998). The reason is that cryptic female choice may operate on a variety of male traits during, or after, copulation, and these may influence the fate of spermatozoa. The "choice," therefore, may involve other mascu- line attributes besides spermatozoa, although male gametes and success- ful fertilizations are the final arbiters of the process. Sperm Competition in Primates Evidence that females mate with multiple partners. Five primary mating systems occur in the Order Primates: monogamy, polygyny, polyandry, multimale-multifemale, and dispersed (Dixson, 1997, 1998a). Monogamous species may not be exclusively monogamous, but adults SEXUAL SELECTION 123 form pairs and raise offspring within family groups. Examples include the South American owl monkeys, 'titi monkeys, and the lesser apes (gibbons) of Southeast Asia. Polygyny refers to a one male-multifemale system, such as occurs in the gorilla and some forest guenons. In certain cases, monkeys live in complex multilevel societies containing large numbers of one male, polygynous units (e.g., hamadryas baboons, geladas, and proboscis monkeys). Polyandry is rare among primates and involves an enduring sexual relationship between one adult female and two or more males. Polyandry has been suggested for some of the cal- litrichid monkeys (marmosets and tamarins) of South America, but their primary mating systems are monogamous. Polyandry has also been reported in a few human societies, as in Tibet (Crook & Crook, 1988), but even in these cases it is not universal, and monogamous marriages also occur. Polygyny has been recorded in many human societies (84% of societies reviewed by Ford & Beach [1952] allow polygynous marriage). In polygynous societies it is typically the most wealthy, or powerful, men who have multiple wives, whereas monogamy is the usual practice for many marriages. This is not to infer that partners are sexually faithful and rigidly monogamous in such cases; extrapair copu- lations occur in other pair-living primates (e.g., in gibbons: Palombit, 1994), so that human beings are not unusual in this regard. However, it is among the remaining two mating systems (multimale-multifemale and dispersed) that we find the greatest evidence of multipartner mat- ings by females. This is the case in the multimale-multifemale groups of many macaques, baboons, and chimpanzees, as well as in the New World capuchins and woolly spider monkeys. Among the nocturnal primates, prosimians, such as bushbabies, pottos, mouselemurs, and many others have "dispersed" mating systems (Dixson, 1987b). Many nocturnal primates do not live in social groups; rather, adults of both sexes occupy dispersed individual, overlapping homeranges. The range of a single male may overlap those of several females. The available evidence indicates that males do not monopolize neighboring females for mating purposes; females may mate with a number of partners (e.g., in galagos, mouselemurs, and ayes-ayes: Dixson, 1998a; Pullen, Bearder, & Dixson, 2000). It is among multimale-multifemale or dispersed mating systems that sexual selection via sperm competition (or cryptic female choice) is most likely to occur in primates. Such selective forces are less pronounced (but by no means absent) in primates whose primary mating systems involve monogamy or polygyny. Relative testes sizes, mating systems, and sperm competition. In some primate species (e.g., the chimpanzee), the testes are very large in relation to adult body weight, whereas in other cases (e.g., in the orang-utan 124 A. DIXSON & M. ANDERSON and the human male), they are of modest size, or relatively small (e.g., the gorilla). Short (1979) was the first to demonstrate that these differences correlate with differences between the mating systems of the apes and man. In multimale-multifemale communities of chimpanzees, females frequently mate with a number of partners and sexual selection has favored the evolution of large testes, containing a greater bulk of the seminiferous tubular tissues required for sperm production. In the gorilla, which is polygynous, females mate primarily with a single domi- nant silverback male in the group; sperm competition pressure is low, and the testes are very small in relation to male body weight. Gibbons, which are primarily monogamous, also have relatively small testes, as do human males, which accords with mankind's primarily monogamous, or polygynous, ancestry. More extensive studies of relative testes sizes and mating systems in the anthropoid primates (monkeys, apes, and human beings) confirmed these findings (Harcourt, HIarvey, Larsen, & Short, 1981), which are summarized in Figure 1. Subsequent work on primates with dispersed (nongregarious) mating systems showed that relative 200 0 Monogamous 2 Multi-male/Multi-female A Polygynous Chimpanzee 100 Anubis baboon 0 Pig-tailed macaque ° Wesembabx 0 Stm-tie Chacma aon Bonnt mwaque p mcqulow 08) Crab-meating macaque Rhesus bor Orang Utan .1.1 Howler monkeyq baboon Goria . Spiderznkey AGdia~~~~~~~sp C.)Vervet 10 - < Proboscis monkey / King colbobs Common langur 4 Mol bbon 9Silver langur Cotton top Lar gibbon A Dusky langur

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