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, seminal 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 successful 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 copulations 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 matings 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

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4 Mol bbon 9Silver langur Cotton top Lar gibbon A Dusky langur tamari1n 0 uirrel monkey

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Body weight (Kg) Figure 1. Relative testes weights and mating systems in anthropoid primates. A logarithmic plot of combined testes weights versus body weight for anthropoids having monogamous, polygynous or multimale-multifemale mating systems. (After Dixson, 1998a; data from Harcourt et al., 1981). SEXUAL SELECTION 125 testes sizes are large in nocturnal prosimians, such as the potto, various galagos, and mouselemurs, in which females mate with multiple partners 'during limited periods of oestrus (Dixson, 1987b, 1995). Large testes sizes are not due to the fact that some primates are seasonal breeders and must concentrate their sexual activities within a limited time span (Har- court, Purvis, & Liles, 1995). Effects of sexual selection upon relative testes sizes have also been confirmed for a number of eutherian mammals (Kenagy & Trombulak, 1986), as well as for marsupials (Rose, Nevison, & Dixson, 1997; Taggart, Johnson, O'Brien, & Moore, 1998). That increases in testes size are due to selective forces favoring males in sperm competition has been demonstrated experimentally in insects (in Scathophaga stercoraria:Hosken & Ward, 2001). Therefore, it is likely that differences between primates shown in Figure 1 are primarily due to differences in sperm competition in the various mating systems. However, the propor- tion of seminiferous tubular tissue (as compared to intertubular tissues) in the testes may also show some phylogenetic variations among the primates, which are poorly understood at present (Dixson, 1998a). Mating systems and spermatozoa. Given the strong correlation between mating systems and relative testes sizes in primates, questions concerning the role of sexual selection in relation to spermatozoa must also be addressed. Well before the proposal of sperm competition and cryptic female choice, Schultz (1938) had found significant differences between the sperm producing tissues of the testes (seminiferous tubules) of different primates. Such findings suggested that certain species with multimale-multifemale mating systems (e.g., macaques) possessed greater quantities of seminiferous tissue and thereby appeared capable of producing larger quantities of sperm than their monogamous counterparts (e.g., gibbons). These early findings lead to comparative studies to investigate how selection pressures may affect the rate of production of sperm and sperm anatomical characteristics. Although sperm production has been measured in relatively few primate species, analysis of data on several key taxa revealed that both the rate of production and size of sperm reserves may be controlled by sexual selection. Indeed, M0ller, (1989) showed that both variables correlate directly with testes size. The differences he observed appear to relate to variations in the mating systems of the species studied, withl species under high sperm competition pressure (e.g., macaque species) showing markedly higher levels of production and reserves than primates under low sperm competition pressure (e.g., Homo sapiens). By examining ejaculate volume, sperm density, and motility M0ller (1989) was also able to demonstrate that those primate species with rela- 126 A. DIXSON & M. ANDERSON tively larger testes produce a greater percentage of motile sperm and larger absolute numbers of motile sperm in their ejaculate. Thus, species under the greatest sexual selection pressure produce not only the greatest quantity ejaculates, but also the highest quality ejaculates overall (e.g., baboons and chimps, having multimale-multifemale mating systems). The prevalence of larger relative testes sizes in those primate species in which females commonly mate with multiple partners, and associated larger volumes of ejaculate and higher ejaculate quality, support Park- er's (1970) sperm competition theory. However, whether such selection pressures also affect sperm morphology (e.g., sperm length or shape of the sperm head) remains a controversial issue. The sperm of nonmam- malian species have been shown to possess many morphological variations. This is especially the case in certain invertebrates (e.g., butterflies and molluscs) in which marked differences in sperm characteristics may relate to different functional roles (e.g., eupyrene (nucleated) and apyrene (non-nucleated) "helper" sperm in butterflies: Trivers, 1985). By comparison with invertebrates, mammalian sperm do not exhibit such marked morphological specializations. An exception is provided by the Virginia oppossum, and some other South American marsupials in which sperm are united at the head end to produce binary spermatozoa (Phillips, 1970; Taggart et al., 1993). However, it has been suggested that selection pressures may be acting upon sperm length in mammals. Sev- eral researchers have demonstrated marked variance across mammalian species, not only in terms of overall length, but also the length of the head, midpiece, and flagellum of the sperm. Although Cummins and Woodall (1985) found total sperm length to be negatively correlated with body mass in general, in subsequent studies in which primate sperm were examined, the investigators failed to demonstrate a relationship between body weight and sperm length (Gomendio & Roldan, 1991; Har- court, 1991). In the absence of any proportional relationship between sperm length and body mass, researchers have focused upon possible explanations for the observed variance in terms of sperm competition. Gomendio and Roldan (1991) postulated that the observed variance might relate to respective primate mating systems. Two hypotheses were put forward: The first was that sperm might be reduced in overall length as a result of selection for greater sperm numbers; the second was that both larger sperm and higher numbers might be selected for. Results of their study supported the second hypothesis with longer sperm being found in primate species with multimale-multifemale or dispersed mating systems. The occurrence of longer sperm was thought to relate to their more rapid swimming ability in the tract of the female, which in turn may lead to a greater chance at fertilizing the ova. SEXUAL SELECTION 127

In a subsequent study, Dixson (1993) supported these findings, although a correlation between sperm length and relative testes size, rather than primate mating system, was found. When primate sperm length was analyzed by Harcourt (1991), he found no correlation between sperm length and mating system. This was also found to be the case when Dixson and Howes reanalyzed the problem, using a 'larger data set (Dixson, 1998a). At the present time, this area of research remains controversial. However, data from Cummins and Woodall (1985) suggest that most of the variance in mammalian sperm length may be accounted for by flagellum length. It would seem advisable, therefore, to repeat those studies, in order to take into account individual measures of not only overall sperm length, but also the length (or volume) of the sperm head, midpiece, and flagellum. More accurate measurements of an adequate number of specimens are required. Not all authorities agree on the types of mating systems exhibited by particular species of primates. This must be taken into account when examining possible relationships between mating systems and sperm morphology. Do human sperm compete? The testes are of moderate size in adult human males, in relation to adult body weight. This does not mean that sperm competition does not occur in human beings, but rather that it is unlikely to have been a major force during human evolution. Baker and Bellis (1995) took a different point of view and proposed that various morphological (or physiological) variants of human sperm have evolved to fulfill different roles in reproduction. "Kamikaze" sperm may occupy the female tract at strategic points and inhibit 'egg-getter" sperm in ejaculates from rival males. Female orgasm functions to "manipulate" ejaculates and preferentially retain sperm under certain circumstances (Baker & Bellis, 1993a). Masturbation, in the human male, is proposed by Baker and Bellis (1993b) as a mechanism to control sperm numbers in the ejaculate and avoid the likelihood of polyzoospermy (Wolf, Byrd, Dandeker, & Quigly, 1984). These ideas have been widely reported in the popular media but have also elicited much serious scientific criti- cism (Birkhead, 2000; Gomendio, Harcourt & Roldan, 1998). Pleiomor- phism is common in human sperm, for example, but there is no evidence that morphologically abnormal sperm fulfill a kamikaze function in sperm competition, or that egg-getter morphs exist. Female orgasm is not known to have any effect on sperm transport or fertility in women (Bancroft, 1989; Masters & Johnson, 1966). Male masturbation is no more frequent in primate species that have far higher sperm counts in their ejaculates than is the case for the human male. Why men should regulate sperm numbers by this means in order to avoid 128 A. DIXSON & M. ANDERSON

polyzoospermy, whereas chimpanzees and many other primates do not is difficult to explain (Dixson, 1998a). The potential window for sperm competition to occur during the human menstrual cycle is very limited and has probably been overestimated by Baker and Bellis (Gomendio et al., 1998). Baker and Bellis allow up to 7 days, whereas Gomendio et al. consider 1.4 days more accurate as the mean time for which sperm sur- vive and retain their fertilizing ability within the female reproductive tract. Mechanisms of sperm competition are best studied in those primates that have multimale-multifemale, or dispersed, mating systems and large relative testes sizes. Research on chimpanzees, macaques, baboons, and galagos is likely to provide more useful insights, therefore, than work on gibbons, gorillas, or human beings, which have primarily monogamous, or polygynous mating systems. The male accessory reproductive organs and sperm competition. The accessory reproductive organs of male primates consist of the prostate and bulbo-urethral glands, which are derived from the urogenital sinus during embryonic development, and the ductuli efferentes of the testis, the epididymis, vas deferens, and seminal vesicles, all of which are derivatives of the mesonephric (Wolffian) duct system. Given that the male's reproductive system serves as a conduit and delivery system for the spermatozoa, it is probable that many, or all, of these organs might be subject to sexual selection (Figure 2). In the case of the seminal vesicles, there are now comparative data to support this hypothesis. In those primate genera in which females commonly mate with multiple partners (multimale-multifemale and dispersed mating systems) the seminal vesicles are significantly larger than in genera in which females mate monandrously (monogamous and polygynous mating systems). These findings are reviewed in Figure 3, in which information on seminal vesicles sizes in 27 primate genera is presented. Likewise, comparative analyses of seminal coagulation across a range of primate genera indicate that coagulum or copulatory "plug" formation is much more prevalent in those cases in which females mate with multiple partners and in which sperm competition pressure is maximal (Figure 4). The seminal vesicles fulfill a number of important functions in reproduction. They produce the bulk of the fluid portion of the ejaculate (60% in the case of the human male: Harper, 1994) and thus provide an important transport medium for spermatozoa. Seminal vesicular secretions have an alkaline pH (pH = 7.2-7.8 in the human male), and this acts to buffer the acidic environment of the vagina and to assist the survival of spermatozoa after ejaculation (Fox, Meldrum, & Baker, 1973; Masters & Johnson, 1966). Seminal plasma contains a huge variety of chemical constituents, such as fructose and prostaglandins. We still SEXUAL SELECTION 129 know relatively little about what roles these constituents might play in sperm competition or cryptic female choice in mammals. However, in fruitflies (Drosophila melanogaster) it is known that secretions of the male's accessory sexual glands can stimulate females to lay more eggs (Chapman, Liddle, Kalb, Wolfner, & Partridge, 1995). In primates, coagulation of semen is due to mixing of protein compo- nents of the seminal vesicular secretion with the enzyme vesiculase, produced by the cranial lobe of the prostate gland (Greer, Roussel, & Austin, 1968; Van Wagenen, 1936). In some species with multimale- multifemale mating systems (e.g., many baboons and macaques) a soft coagulum is produced, which comprises 55%-68% of the ejaculate

Figure 2. Dissection of the reproductive tract of an adult male orang-utan (Pongo pyg- maeus) to show the major organs. Blad = bladder; BM = bulbocavernosus muscles; Bu = bulbo-urethral gland; CE = cauda epididymis; IM = ischiocavernosus muscle; Pe = penis; Pre = prepuce; Pro = prostate; Sv = seminal vesicle; Te = testis; Ur = urethra; Ut = ureter, Vas = vas deferens. 130 A. DIXSON & M. ANDERSON

A. Monogamy 4 - CALLITHRIX SAGUINUS 2 CALLICEBUS AOTUS P1HECIA SYMPHALANGUS

B. Polygyny 2 1 |THEROPITHECUS

E LA HOMO Z O E_

o C. Multimale / multifemale

* 9 LEMUR ATELES 6- BRACHYTELES SAIMIRI CERCOCEBUS 3: MANDRILLUS MACACA CEBU_S: PAPIO ILAGOTHIRL PAN

D. Dispersed

NYCTICEBUS 4- LORIS PERODICTICUS 2 - ARCTOCEBUS MICROCEBUS DAUBENTONIA I PONGO 0 - I :1 Vestigial Small Medium Large SEMINAL VESICLES

Figure 3. Seminal vesicle sizes and mating systems in 27 primate genera. Seminal vesicles are rated as vestigial, small, medium-sized, or large. Mating systems are classified as monogamous, polygynous, multimale/multifemale, or dispersed. Numbers of genera in each category are shown as open bars, with the genus names included within each bar. *Includes Eulemur. (After Dixson, 1998b). SEXUAL SELECTION 131

A. Monogamy 8 ,

CALLITHRIX AOTUS SAGUINUS 4. CALLIMICO NOMASCUS 2. HYLOBATES SYMPHALANGUS

0 -i B. Polygyny 4-

ERYTHROCEBUS 2 - GORILLA

A _ IIHOMO P. HA 0 C. Multimale / multifemale 6 1 I LEMUR I a7 MACACA EULEMUR 4 - PAPIO ATELES CERCOCEBUS BRACHYTELES 2- MANDRILLUS M. ARCTOIDES MIOPITHECUS PAN 01 D. Dispersed 6 -1 MICROCEBUS 4i ARCTOCEBUS LORIS 2- NYCTICEBUS GALAGO

O - 1 2 3 4 SEMEN COAGULATION RATING

Figure 4. Seminal coagulation scores and mating systems in 26 primate genera. Seminal coagulation is rated on a 4-point scale, with 1 = coagulation absent, and 4 = a solid copulatory plug is formed. 132 A. DIXSON & M. ANDERSON

(Wildt, 1986). The coagulum contains spermatozoa (30%-70% of all gametes in the ejaculate in the case of the rhesus monkey: Hoskens & Patterson, 1967; Roussel & Austen, 1967), and these are gradually released as the coagulum liquifies. Some primates, such as the chimpanzee, stumptail macaque, and woolly spider monkey produce a more substantial, rubbery copulatory "plug." The functions of mammalian copulatory plugs have been much debated and remain controversial. However, plug formation, as with coagulum formation, may serve to protect spermatozoa from the hostile (acidic) environment within the female's vagina. Plugs may also serve to maintain a sperm-rich fraction of the ejaculate in contact with the os cervix, to prevent backflow of semen and assist sperm transport (Dixson, 1998a). The larger sizes of the seminal vesicles and greater prevalence of coagulum/plug formation in those primates in which females mate with multiple partners (Fig- ures 3 and 4) may, therefore, be adaptive in the context of sperm competition. Seminal vesicles are potentially physiologically "costly" structures. Thus, the production of proteins, fructose, and numerous other biochemical constituents by the seminal vesicles may impose a physiological burden (or cost) upon the male and especially so if the vesicles are very large. Reduction in their size may, therefore, have occurred in some primates that are monogamous, or polygynous, such as Callicebus,Aotus and Symphalangus (Figure 3). Sexual selection and penile morphology. Studies of the reproductive anatomy of primates have revealed that their genitalia can be extremely specialized (Anderson, 2000; Dixson, 1987b; Hill, 1958). This is particu- larly true of penile morphology, which differs markedly even between very closely related species within a single genus (Anderson, 1998; Dix- son, 1987b, 1991a; Hill, 1953). Morphological variations include differences in length, complexity of distal structures (e.g., presence, size, and shape of keratinized spines and presence or absence of the os penis or baculum), and other characteristics. Although such traits vary widely between different primate species, levels of intraspecific variation for any given penile feature are relatively low. As a result, penile morphology is a powerful diagnostic tool in primate classification, especially in certain nocturnal prosimian primates, which are very difficult to classify using gross anatomy alone (Anderson, 2000; Dixson, 1989, 1995). An evolutionary explanation for penile complexity remained problem- atic until Eberhard (1985) wrote his volume entitled Sexual Selection and Animal Genitalia, in which he described sexual selection via cryptic female choice. Prior to this treatise, four alternative hypotheses had been advanced to explain genitalic complexity. Each is considered briefly in order to highlight the significance of Eberhard's contribution. SEXUAL SELECTION 133

1. The 'lock and key" hypothesis proposes that males of certain species have developed complex genitalia in order to mesh with equally complex female structures that recognize only the correct permutation; or "key," provided by the male of the same species (Mayr, 1963). This mechanism reduces the likelihood of interspecific copulations and thereby acts as an isolating mechanism. However, given that selection is thought to favor isolating mechanisms that operate before genital contact and that examination of female anatomy has (in many cases) revealed very little evidence for development of complementary adapta- tions of vaginal morphology, this idea has lost support. 2. A second hypothesis is based upon the concept of "genitalic recognition." It is that females recognize conspecific males via stimulation received during copulation. This is essentially a variant of the lock and key hypothesis, and is subject to the same criticisms. It was thought that such appropriate recognition might enhance fertility. However, although some mammals (e.g., the rat) show evidence of copulation- induced neuroendocrine changes resulting in support of the corpus luteum during pregnancy (Adler, 1969), primates (which are sponta- neous ovulators) do not require coital stimulation for support of the corpus luteum. 3. Mayr (1963) suggested that penile complexity results from pleiotropic, or incidental genetic effects. He proposed that extremely variable genital characteristics arise as a side effect of genetic changes in other systems that were favored by natural selection. However, the lack of pleiotropic effects in other organs, as well as other criticisms raised by Eberhard (1985), effectively refute this idea. 4. The mechanical conflict of interest hypothesis is based upon the idea that males and females have conflicting interests during copulation. It is that males develop penile complexities in order to restrain the female, or force sperm to be accepted by her (Lloyd, 1979). Again, although there are cases of such mechanisms in some insects, primates show no such genitalic devices. Given the inherent limitations of these proposals, Eberhard's (1985) hypothesis concerning cryptic female choice offers a more credible explanation for observed penile complexity. Eberhard suggested that penile complexity is likely to be greater in species in which any given female mates with a number of different males. In such cases the penis may function as an 'internal courtship device" encouraging sperm transport and fertilization. As female anatomy offers many opportuni- ties for cryptic "choice" (e.g., anatomical and physiological barriers in the cervix, uterus, and uterotubal junction), any small adaptive features of male genital morphology (and indeed copulatory behaviour) might 134 A. DIXSON & M. ANDERSON become subject to evolutionary change. In a study of penile morphology and mating systems in primates, Dixson (1987b) examined 130 primate species in order to test the validity of Eberhard's hypothesis. Qualita- tive measures were made (length of pars libera, length of os penis, size of keratinized spines on distal portion of the penis, and complexity of the distal end of the penis), along with comparisons of different mating systems (monogamous, polygynous, multimale-multifemale, and dispersed). The resultant data supported Eberhard's predictions, with multimale-multifemale species showing longer penes, larger bacula, and higher overall complexity of the distal penis. Subsequent observation of primates with dispersed mating systems revealed even higher levels of complexity, a finding that was further borne out in a quantitative study of penile morphological characters in galagos (Anderson, 2000). Find- ings from these latter studies allow for speculation on how cryptic female choice may have played a role in the evolution of specific penile characters. Indeed, only by considering the possible copulatory function of each structural character (specifically penile spines, distal penile complexities, and the baculum) is it possible to begin to suggest the possible effects of sexual selection in each case. Keratinized penile spines occur on the glans penis in prosimians, monkeys, and apes, and represent a primitive character of the Order Primates. Penile spines are made up of layers of keratinized material and occur as either simple, single-pointed conical or elongated structures, or as multipointed complexes. As discussed, spines also exhibit marked interspecific variations in size and shape and as such can be further classified into three different categories (Dixson, 1998a): Type 1: simple spines: small single pointed structures of moderate length, occur widely amongst primates (e.g, Callithrixjacchus); Type 2: robust simple spines: single pointed structures but much enlarged and often thickened at the base, occur most commonly in prosimians and a few anthropoids (e.g., Galagoidesdemidoff); Type 3: complex spines: multi-pointed structures typically of large size, occur in prosimians only. The number of points can vary from two or three per spine (e.g., Galago garnettii) up to six (e.g., Microcebus murinus). In evolutionary terms, type 1 spines appear to represent the primitive or unspecialized condition. Type 1 spines, which are situated above tactile receptors in the dermis of the glans penis, enhance tactile signals required to achieve intromission and/or ejaculation when deflected during pelvic thrusting (Dixson, 1991a). Greater complexity of penile spines may have resulted from increasing the size of type 1 spines and/or fusing two or more spines in order to produce complex struc- SEXUAL SELECTION 135 - tures. Further complexity results from the occurrence of different spine types on different areas of the glans. It is possible that the various spines might play different roles within a single species. Some spines might assist in imparting tactile stimulation to the female and thus facilitate neuroendocrine responses affecting sperm transport. Spines may assist in the removal of coagulated semen or copulatory plugs deposited by previous matings, but there is no evidence for such effects in primates. Finally,,there may be selection for spines that have a mechanical role, such as gripping the walls of the vagina to facilitate a copulatory lock. The os penis or baculum, like keratinized spines, is thought to be a primitive character because it occurs in most primate species. The baculum arises from ossification of the distal region of the corpora cavernosa and extends forwards into the glans penis. The development of the baculum is affected by androgens and the bone enlarges during puberty. Interspecific comparisons reveal that both length and shape of the baculum vary considerably. Some species have greatly elongated bacula (e.g., nocturnal prosimians, such as Galago, Daubentonia, and Perodicticus), whereas in others it is greatly reduced or entir'ely absent (as in spider monkeys, tarsiers, and man). When compared with the prosimians and Old World monkeys, the New World monkeys have relatively smaller bacula. Although differences can be partly explained in terms of phylogenetic relationships, the enormous variation observed even within certain genera necessitates examination of alternative explanations. For example, there is a correlation between the occurrence of an elongated baculum and copulatory patterns that involve prolonged intromission (Dixson, 1987a). Species with single prolonged intromission copulatory patterns have significantly longer bacula than those that utilize either single brief intromissions or multiple brief intromissions (Figure 5). Additionally, primates with elongated bacula also tend to be species in which intromission is maintained into the postejaculatory period. All such primates exhibit either multimale-multifemale or dispersed mating systems. It is most likely, therefore, that the elongation of the baculum relates to its various functions during prolonged intromission. Several different roles have been proposed (Dixson, 1998a; Long & Frank, 1968; Patterson & Thaeler, 1982), which may explain the evolution of diversity observed. Hypotheses include helping to gain intromission, providing added rigid- ity during intromission, aiding the positioning of copulatory plugs (e.g., in Macaca arctoides), assisting the stimulation of the female during copulation (in order to elicit a neurological response important for fertility), and facilitating sperm transport into the os cervix during copulation. 136 A. DIXSON & M. ANDERSON

Copulatory patterns and ejaculatory frequencies. Four copulatory patterns have been recorded for male primates (Dixson, 1998a) using a modified version of Dewsbury's (1972) schema for classifying the copulatory behavior of male mammals. In many species, such as marmosets, owl monkeys, and chimpanzees, copulation involves a single relatively brief intromission, accompanied by pelvic thrusting movements. More complex copulatory patterns involve either a series of intromissions, with pelvic thrusting (as in rhesus and Japanese macaques, red colobus monkeys, and chacma baboons) or a single prolonged intromission during which thrusting movements are of limited duration or occur sporadically during the mount (e.g., in woolly spider monkeys, orang-utans, and galagos). Dewsbury and Pierce (1989) concluded that a "genital lock" does not

1.5- ---g32

3 / z -J 1.0

0 0.5- o~~~~~~~~~~1 /

2.0 2.5 3.0 3.5 4.0 LOG BODY WEIGHT

Figure 5. Logarithmic plot of baculum length in relation to patterns of copulatory behaviour in 34 species. C = Species with long intromission times and/or postejaculatory main- tenance of intromission. 0 = Species in which copulation is usually brief and intromission is terminated promptly after ejaculation. Principal axes are plotted separately for the two groups. Two additional species are plotted for which only anatomical data are available: A Perodicticuspotto; 0 Daubentonia. Species studied are as follows: 1. Galago garnettii, 2. G. demidoff7 3. G. senegalensis, 4. Loris tardigradus, 5. Macaca arctoides, 6. Lemur catta, 7. V. variegata, 8. Saguinus oedipus, 9. S. fuscicollis, 10. Leontopithecus rosalia, 11. Cal- limico goeldii, 12. Callithrix jacchus, 13. C. argentata, 14. Aotus lemurinus, 15. Saimiri sciureus, 16. Cebus apella, 17. Cercopithecus aethiops, 18. C. mitis, 19. Miopithecus talapoin, 20. Erythrocebus patas, 21. Cercocebus atys, 22. C. albigena, 23. Mandrillus sphinx, 24. M. leucophaeus, 25. Papio ursinus, 26. P. anubis, 27. P. hamadryas, 28. Thero- pithecus gelada, 29. Macaca sylvanus, 30. M. nemestrina, 31. M. nigra, 32. M. fascicularis, 33. M. mulatta, 34. M. fuscata. '-' = fossil adapid described by Von Koenigswald. (After Dixson 1987b). SEXUAL SELECTION 137 occur during copulation in primates. However, there is some evidence that locking may occur in some primates that employ a single prolonged intromission pattern of copulation (e.g., stumptail macaques: Lemmon and Oakes, 1967; Garnett's galago: Dixson, 1998a). If confirmed, the occurrence of genital locking during a prolonged intromission would con- stitute the fourth copulatory pattern attributable to primates. The evolutionary significance of prolonged intromissions is not known for certain, but some hypotheses may be advanced. Firstly, prolonged intromission occurs in small-bodied nocturnal prosimians (such as galagos, lorises, and aye-ayes) that are arboreal. Among the diurnal primates, only a few relatively large-bodied arboreal monkeys (e.g., the woolly spider monkey and the orang-utan) copulate for extended periods. This pattern has not been recorded for small-bodied diurnal monkeys, or for terrestrial species, with the exception of the stumptail. One explanation for this may be that predation pressure has selected against the evolution of prolonged intromission patterns in terrestrial primates, and in small-bodied, arboreal monkeys that are active during the day (Dixson, 1991b). Prolonged intromissions may function as a form of mate-guarding behavior, for instance in greater galagos, among whom copulations can last for more than an hour and in which -the duration of female recep- tivity is reduced as a result of lengthy, uninterrupted matings (Dixson, 1998a). Bouts of pelvic thrusting occur at intervals during prolonged intromissions in Galago garnettii. Thus, it is possible that multiple ejaculations occur during a single mount, although definitive proof of this is lacking. All of these possibilities-mate-guarding, tactile stimulation of the female, and occurrences of multiple ejaculations-might have favored the evolution of prolonged single intromissions. It may be significant, therefore, that this copulatory pattern has only been reported in primate species that have dispersed, or imultimale-multifemale mating systems; none of the polygynous, or monogamous, species possess such a copulatory pattern. Some galago species may copulate for over an hour, for example, and prolonged intromissions occur in woolly spider monkeys (up to 8 minutes), woolly monkeys (up to 14 minutes), and orang-utans (median duration = 14 minutes). If it is objected that human beings engage in prolonged copulations and have polygynous, or monogamous mating systems, then some facts concerning human copulatory behavior may require reevaluation. Kinsey, Pomeroy, and Martin, (1948) recorded that 'perhaps three quarters of all males" (p. 580) in their sample reached ejaculation in less than 2 minutes during intercourse. Is it possible, therefore, that prolonged copulations might be the result of cultural evolution in Homo sapiens 138 A. DIXSON & M. ANDERSON and that the primitive pattern for our species might consist of a relatively brief intromission of less than 2 minutes? Cryptic Female Choice and Coevolution of Male and Female Genitalia Cryptic female choice in invertebrates. Eberhard's hypotheses concerning cryptic female choice and genitalic evolution (Eberhard, 1985, 1996) derive from research on insects and other invertebrates. Research on invertebrates has advanced much more rapidly than comparable work on mammals. It will be useful to review some data on mechanisms of cryptic female choice in invertebrates before considering the limited information available on primates. In many species, males impart stimulation to females in various ways during copulation besides the tactile stimulation provided by genitalic contact. In the red flour beetle (Tribolium castaneum), for example, the male rubs the lateral edges of the female's wing covers (elytra) with the tarsi of his legs. Males in which the tarsi are removed continue to copulate and make rubbing movements but are not able to contact the edges of the female's elytra. Such males are less successful in fertilizing ova. Edvardsson and Arnqvist (2000) interpreted this result as showing that 'female perception of male copulatory courtship behaviour, rather than male behavior per se, apparently governs the fate of sperm competing over fertilizations within the female, showing that copulatory courtship is under selection by cryptic female choice" (p. 559). In Drosophila melanogaster, both sexes play a role in determining which sperm are successful in fertilizing ova when females mate with multiple partners. Females retain sperm in specialized sacs (spermatothecae), and gametes from more than one male may be stored in this way. Clark, Begun, and Prout (1999) have shown that the success of a particular male's sperm is influenced by the genotype of the female. The authors suggested that female fruitflies may be able to detect and avoid gametes of related males by detecting chemical cues in their accessory sexual secretions. Coevolutionary processes may be at work between the sexes, and these 'may be responsible for the rapid rate of molecular evolution of genes encoding seminal proteins" (p. 219). In the beetle, Chelymorpha alternans, the male possesses a long flagellum on the intromittent organ, and this is threaded into the female's spermatothecal duct during mating. Sperm move along the flagellum to reach the female's spermatotheca. Flagellum length correlates with success in siring offspring, whereas ejection of a male's sperm by the female is increased if his flagellum has been shortened experimentally (Eberhard, 1996). Female ejection of sperm from the spermatotheca also plays a role in influenc- ing male reproductive success in some damselflies; it is the female's per- SEXUAL SELECTION 139

ception of copulatory stimuli received from males that determines if she will eject sperm from stores deep within her reproductive tract (Cor- doba-Aguilar, 1999). The results of studies on several other invertebrate species also indicate that cryptic female choice, as well as sperm competition, may operate to determine male reproductive success in species in which females mate with multiple partners (e.g., in the yellow dung fly, Scathophaga stercoraria:Ward 2000; the cowpea weevil, Callosobruchus maculatus: Wilson, Tubman, Eady, & Robertson, 1997 and the ascidian, Beroe ovata: Carre, Rouviere, & Sardet, 1991). Cryptic female choice in primates. Eberhard's hypothesis predicts that penile morphologies should be most complex in those species in which females mate with multiple partners during the fertile period. We have seen that this is the case in primates, and that males tend to have more complex penile morphologies in species that have multimale-multifemale, or dispersed, mating systems. Less morphologically complex genitalia are more typical of monogamous, or polygynous, primates (Dixson, 1987b; Verrell, 1992). Specializations include the overall length of the penis, or baculum, and complexity of distal penile morphologies, which can be pronounced in forms such as galagos, lorises, and macaques. If cryptic female choice promotes sexual selection for these traits, how might this occur? There is very little experimental data to address this question in primates, but some possibilities are worthy of consideration. Numerous factors influence the survival, storage, or transport of spermatozoa within the female reproductive tract in primates. Some of these are shown, in diagrammatic form, in Figure 6. The first example presented in that diagram concerns the size and depth of the female 'sexual skin swellings" that occur in various Old World monkeys (e.g., baboons, talapoins, and mangabeys), as well as in the chimpanzee and bonobo. These swellings are maximal in size during midmenstrual cycle when females are most likely to ovulate and conceive. Swellings are visually arousing and sexually attractive to males (Girolami & Bielert, 1987), and they probably evolved as visual indicators of female reproductive fitness. However, a secondary effect of the swelling is to greatly increase the length of the female's vagina during the peri-ovulatory period of her cycle, when fertile matings can occur. In species possessing swellings, females typically mate with a number of males, so that sperm competition is likely. However, for such competition to even be an issue, males must first position their ejaculates as advantageously as possible within the female's reproductive tract. In practice this requires positioning of sperm at the cervical os, so that they may migrate through the cervix, into the uterus, and thence to higher portions of the female tract. In the 140 A. DIXSON & M. ANDERSON

.9 11 -8

Figure 6. Some of the factors that influence the transport, or storage, and viability of spermatozoa within the female reproductive tract. 1. Sexual skin swelling and vaginal elongation affects the male's ability to achieve maximal insertion before ejaculation. 2. Myometrial and vaginal contractions affect rapid sperm transport. 3. Low vaginal pH reduces sperm survival; semen buffers vaginal pl-I. 4. The physico-chemical properties of cervical mucus alter during the cycle and affect sperm transport through the cervix. 5. Cervical crypts act as reservoirs for storage and gradual release of spermatozoa. 6. Spermn are transported through the uterine cavity towards the uterotubal junction. 7. Filtering and further selection of sperm can occur at the uterotubal junction. 8. Temporary storage of spermatozoa occurs in the isthmus of the oviduct. 9. Sperm capacitation and the hyper- activation of swimming movements reaction occur in response to oviductal stimuli. 10. The ovum and its vestments exert selective effects upon sperm and may release chemical cues that affect spermatozoa. 11. Oviductal length may be the greatest in species in which sperm competition is most intense. SEXUAL SELECTION 141 chimpanzee, genitai measuremenits have shown that vaginal depth increases by up to 50% when females are at full swelling and that under these conditions males vary in their ability to contact the cervical os during intromission (Dixson & Mundy, 1994). The exceptionally long, filiform penes of the chimpanzee and bonobo probably evolved, therefore, as morphological responses to the very deep sexual skin swellings of females (Dixson, 1998a). The same may be true in some other primates that have prominent swellings (e.g., red colobus monkeys and mangabeys). The important point is that coevolution of the male and female genitalia has occurred. Sperm competition does not take place in isolation from female influences, and the female's reproductive anatomy and physiology imposes selection pressures upon competing males. The specialized penile morphologies of some primates may be due, at least in part, to selection pressures determined by the female and not solely by intermale competition. Likewise, the large seminal vesicles of primates -having multimale-multifemale, or dispersed, mating systems may have evolved in tandem with mechanisms in the female tract that determine sperm survival and usage (Figure 6). In reality, because of such coevolution, it may be very difficult to treat mechanisms of sperm competition and cryptic female choice as if they are separate and unre- lated processes. A huge number of questions remain to be addressed regarding the effects of sexual selection upon the evolution of genitalic and copulatory mechanisms in mammals. As an example, in a small sample of mammals (11 species) examined by Gomendio and Roldan (1993) it was possible to demonstrate a positive correlation between oviductal length and sperm numbers. The occurrence of long oviducts (relative to female body size) correlates with the production of high sperm numbers and sperm competition among males. These findings are intriguing and should be replicated using a larger sample of mammalian species. At the present state of knowledge, it seems likely that sperm competition has played' a significant role in the evolution of reproduction in primates, as in some other animal groupq. The question of cryptic female choice is more controversial, but there are intriguing indications for its occurrence in various invertebrates. The way lies open for further testing of Eberhard's theory using comparative studies of reproductive anatomy and physiology in monkeys, apes, and human beings. References Adler, N. T. (1969). Effects of the male's copulatory behavior on successful pregnancy of the female rat. Journal of ComparatiuePhysiological Psychology, 69, 613-622. - Anderson, M. J. (1998). Comparative morphology and speciation in galagos. Folia Prima- tologica, 69(Suppl. 1), 325-331. 142 A. DIXSON & M. ANDERSON

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TITLE: Sexual Selection and the Comparative Anatomy of Reproduction in Monkeys, Apes, and Human Beings SOURCE: Annu Rev Sex Res 12 2001 WN: 0100106539005

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