Adams Apple

'It is interesting to conjecture as to the appearance and mode of life of the ancestors of present day Man, and in such a study much assistance may be derived from an examination of the larynx.'

Negus (1949)

An obvious anatomical sex difference in adult humans concerns the size and shape of the larynx, with resultant differences in vocal pitch; this is usually deeper in men than in women. These structural and vocal sex differences develop during puberty when, under the action of testosterone, the cartilages and muscles of the male larynx enlarge and the vocal cords increase in length. The thyroid cartilage, the largest of the nine cartilages which make up the larynx, becomes especially prominent in some males, causing a bulge to appear in the mid-line at the front of the neck; this is the pomum Adami, or Adam's apple (Figure 8.1).

Darwin (1871) was well aware of this sex difference in Homo sapiens, and noted parallels in the greater size of the larynx and deeper vocalizations of various male mammals. He considered that 'man appears to have inherited this difference from his early progenitors. His vocal cords are about one third longer than in woman, or than in boys.'

In this chapter, I shall examine the question of whether sex differences in laryngeal anatomy and vocal pitch can tell us anything about the likely mating system of our early progenitors. From a comparative standpoint, an important question concerns the extent to which such sex differences correlate with mating systems in other mammals. Darwin knew that in cervids, mature stags exhibit marked enlargement of the larynx and emit powerful roaring vocalizations during the annual mating (rutting) season. Yet, surprisingly, he was unable to establish any firm connection between sexual selection and the evolution of roaring displays in stags, saying that 'As the case stands, the loud voice of the stag during the mating season does not seem to be of any special service to him, either during his courtship or battles, or in any other way.' Modern research has shown, however, that the roar of a red deer stag (Cervus elaphus) may transmit information about that individual's dominance status, strength, and reproductive potential. Roaring is valuable as a distance signal to rival males as it may transmit information about body size (Reby and McComb 2003) and probable fighting ability (Clutton-Brock and Albon 1979). The stag's roars can also evoke physiological responses in females, serving to synchronize their oestrus cycles. Putman (1988) states that deer species in which stags compete to hold harems (i.e. polygynous species such as the red deer) are characterized by the occurrence of striking male vocal displays during the rutting season. 'In harem holding species, the call is essentially male competitive display; in stand holding species the call serves the double function of male challenge and female attraction.' The calls made by stags vary a great deal, depending upon the species concerned, and range from high-pitched whistles (sika), roars (red deer), and deep bellows (wapiti and bull moose), to belches and groans (fallow deer). 'Whatever the actual tone, however, the call always has a curious carrying quality' (Putman 1988).

Diagram Sex HumanThyroid Cartilage

Figure 8.1 The human vocal tract in schematic sagittal section, together with views of the thyroid cartilage (arrowed in the upper diagram) and an illustration of sex differences in the angle of the thyroid cartilage (lower diagram). Source: From Balaban (1994); after Dickson and Maue-Dickson (1982).

Given that the larynx is markedly sexually dimorphic in adult human beings, and that testosterone stimulates laryngeal growth during puberty (Beckford et al. 1985; Hollien, Green and Massey 1994), it is important to determine whether sexual selection has influenced the evolution of these traits. Firstly, we may ask whether the human voice conveys any information concerning an individual's hormonal or physical status. The answer to these questions appears to be 'Yes'. Indeed, many years ago Eberhard Nieschlag showed that masculine vocal register, body condition, and circulating testosterone are correlated in the human male. Thus, he found that bass singers have higher testosterone/oestradiol ratios and ejaculatory frequencies than tenors, as well as being, on average, taller and more athletic in their physique (Figure 8.2). Subsequently, Dabbs and Mallinger (1999) reported that men who have deeper voices also exhibit significantly higher levels of salivary testosterone. Low-pitched male voices are judged as more pleasant or attractive by women in at least some studies (Collins 2000; Feinberg et al. 2005). Bruckert et al. (2006) found that women tended to find lower-pitched men's voices more pleasant, but also that they based their judgements on changes in intonation and increases in temporal pitch. The men in these studies were recorded as

Testosterone / oestradiol

Tenor Baritone Bass

Figure 8.2 Differences in molar ratios of testosterone and oestradiol, and frequencies of sexual activity (ejaculatory frequencies) in male singers (tenor, baritone, and bass) aged 20-40 years. Source: Based on data from Nieschlag (1979).

Tenor Baritone Bass they spoke a series of five vowel sounds. The series was spoken only twice, by twenty-six men ranging in age from 18-32 years. Remarkably, women were able to assess accurately the ages and body weights of these men on the basis of their voices alone. Although they failed to accurately estimate the heights of the men concerned, body weight and height were positively correlated in these same subjects, and taller men also had significantly lower vocal frequencies. Thus it seems reasonable to conclude that masculine voice tone can convey accurate information to women concerning an individual's age, body size, and androgenic status. Women find deeper male voices more pleasant and attractive.

Deeper voices may also be linked to physical and social dominance in men. In a study conducted by Puts, Gaulin, and Verdolini (2006), men rated competitors as more socially and physically dominant if their recorded voices were manipulated so as to be lower in pitch. These investigators also found that men who regarded themselves as physically dominant tended to lower their own voices when responding to recordings of male competitors.

Other studies have shown that women also rate deeper, masculine voices as being more dominant (Feinberg et al. 2005). The pitch of men's voices

Ejaculations

Tenor Baritone Bass

Figure 8.2 Differences in molar ratios of testosterone and oestradiol, and frequencies of sexual activity (ejaculatory frequencies) in male singers (tenor, baritone, and bass) aged 20-40 years. Source: Based on data from Nieschlag (1979).

tends to be about half as high as that of women (Titze 2000) and vocal pitch correlates with hormonal, physical, and behavioural traits which affect inter-male competition and female mate preferences. Sex differences in the anatomy of the vocal tract and in voice quality in human beings are thus likely to be due to sexual selection, and not simply to sex differences in adult body size. As Darwin suggested, these effects upon the larynx and human voice are likely to be ancient characteristics, deriving from the early progenitors of Homo sapiens.

It is important to note that it is the pitch of the voice and sex differences in vocal pitch which are relevant here. Such traits are likely to have arisen before the origin of human language and may have been present in the australopithecines, or in the earliest representatives of the genus Homo.

There is evidence that vocal pitch is related to measures of male reproductive success in human beings. Thus, Apicella, Feinberg, and Marlowe (2007) were able to show that among the Hadza of Tanzania, who still live as traditional hunter-gatherers, men with the deepest voices father significantly more children.

In order to further grasp the relevance of sex differences in vocal traits to discussions of human mating systems and their evolution, it is helpful to consider how these traits relate to the mating systems of the extant non-human primates. Are there sex differences in vocal tract anatomy and associated differences in vocal pitch in male and female monkeys and apes? If so, do these differences relate in a consistent fashion to the occurrence of monogamy, polygyny, or multi-male/multi-female mating systems among the anthropoids? The larynx is composed of the same cartilaginous elements in monkeys and apes as it is in H. sapiens: as an example, the larynx of a chimpanzee is shown in Figure 8.3. However, the relative sizes of these cartilages and their associated musculature differ between species and, additionally, there are extensions of the larynx called laryngeal air sacs. These can be enormous in some cases (as in the orangutan and gorilla) and they are often inflated during vocal displays. All primates possess a pair of lateral ventricular air sacs and these are especially well developed in the great apes and in the siamang. Human beings are no exception to this rule, but the human lateral laryn-geal sacs are very small, being situated in the wall of the larynx between the (upper) false vocal cords and (lower) true vocal cords in both sexes. These pouches are richly supplied with mucous secreting glands; this mucous acts as a lubricant for the vocal cords. The situation is very different in the great

Corpus hyoideum Cornu minus (hyale)

Lamina thyreoidea

Membrana cricothyreoidea Cartilago cricoidea

Corpus hyoideum Cornu minus (hyale)

Lamina thyreoidea

Membrana cricothyreoidea Cartilago cricoidea

Membrana Thyreoidea

Figure 8.3 Lateral view of the larynx of a chimpanzee (Pan troglodytes), dissected to show the arrangement of the laryngeal cartilages. Source: From Starck and Schneider (1960).

Cornu branchiale I.

Membrana thyreohyoidea

Cornu superius Arytenoid verkalkter Knorpel im Thyreiod

Cornu inferius

Figure 8.3 Lateral view of the larynx of a chimpanzee (Pan troglodytes), dissected to show the arrangement of the laryngeal cartilages. Source: From Starck and Schneider (1960).

apes, for in all cases the lateral ventricular sacs are much enlarged and extend into the neck, chest, and axillae. This is especially the case in the adult male gorilla and orangutan, in which the laryngeal sacs are also much better developed in adult males than in females (Figures 8.4 and 8.5).

Mature male orangutans emit spectacular, deep-pitched long calls which are audible for over 1 km in the rainforest. Males inflate their vocal sacs during these displays, which may last for 1-2 min, and are thought to serve primarily for communication between individuals, as orangutans are widely dispersed across the forest canopy (Mitra Setia and Van Schaik 2007). The massive size, striking cheek flanges, and other secondary sexual adornments of adult male orangutans are indicative of the effects of evolution by sexual selection, such as occurs among polygynous primates. Because these apes are relatively non-gregarious and do not form permanent social groups, it is especially important for adult males to be able to communicate over long distances. The development of the laryngeal sacs and long call is significant in this respect. In Chapter 3 the occurrence of delayed secondary sexual development in non-flanged adult male orangutans was discussed in relation to their mating strategies and the relevance of sperm competition in orangutan reproduction. Non-flanged males not only lack the striking visual secondary sexual adornments and massive size of territorial males, they also have a smaller larynx, lack the throat sac, and do not give long calls. Development of all these traits is, presumably, influenced by testosterone, or by greater target organ sensitivity to testosterone, in those males which progress to become fully flanged individuals.

Silverback male gorillas also possess an extensive array of air sacs derived from the paired lateral laryngeal sacs (Figure 8.5). Schaller (1963) noted that silverback mountain gorillas make use of the laryn-geal sacs during their chest-beating displays. The chest-beats, which resemble hollow 'pock-pocking' sounds, may carry for as much as 2 km. Schaller also observed that 'the prominent air sacs also act as resonators, for their sudden inflation on each side of the throat is sometimes readily apparent before the chest-beat.' Gorillas are polygynous and the adult male's chest-beating display serves a variety of functions, including inter-group communication and intimidation of potential rivals. Although adult

Figure 8.4 Dissection of an adult male orangutan (Pongo pygmaeus) to show the extent of the (inflated) laryngeal sacs. These sacs are inflated during the male's 'long-call' displays.

Source: From Dixson (1998a); after Hill (1972).

Figure 8.5 Chest-beating display of an adult male western lowland gorilla (Gorilla g. gorilla) and a dissection of the laryngeal sacs, which are inflated to act as resonators during the display.

Source: From Dixson (1981).

females and juveniles also chest-beat, they produce much duller sounds which are not audible over long distances. Silverbacks may also vocalize when alarmed or aggressive to produce explosive, deep-throated roars. Again, immature males are unable to emulate the depth of pitch and vocal power of silverbacks, presumably because the larynx and associated musculature is not yet fully developed. Schaller (1963) considered that black-backed (adolescent) males 'were at an awkward age, vocally speaking, in that their voices appeared to be changing. Thus young males screamed when angry, and the older ones produced rather squeaky roars. Only silver backed males were heard to emit the full roar, the clear hooting preceding the chest beat, and the staccato copulation call.' Thus, black-backed males are probably at a stage where the larynx is enlarging, and the vocal cords are lengthening during puberty, a situation which is homologous with the breaking of the voice which occurs in human males at this time.

Chimpanzees and bonobos also exhibit large extensions of the lateral laryngeal sacs. However, the larynx is not markedly sexually dimorphic in these species and nor does the pitch of the voice differ so greatly between the sexes. Both male and female chimpanzees emit loud 'pant-hoots' when communicating over a distance (Marler and Hobbett 1975). These vocalizations are important as contact calls between the sub-groups which make up the multi-male/multi-female, or fusion-fission communities in which chimpanzees live. There is thus no equivalent among chimpanzees of the highly sexually dimorphic displays used by orangutans and gorillas.

In the smaller apes or gibbons (Hylobatidae), the principal mating system is monogamous, and adults of both sexes engage in complex vocal 'duets' which exhibit interesting inter-specific variations (Haimoff 1984). Only the siamang (Hylobates (Symphalangus) syndactylus) possesses prominent lateral laryngeal sacs, but in this case they are equally developed in adults of both sexes. Males and females inflate the sacs during their prolonged displays (Figure 8.6). It is likely that the duets produced by gibbon pairs may transmit complex information between groups; such distance communication has apparently undergone positive selection in the rainforest

Figure 8.6 A siamang (Hylobates (Symphalangus) syndactylus) with the vocal sac inflated. Both sexes possess large lateral laryngeal sacs, which are inflated during vocal duets. Source: Author's drawing from a photograph in Rowe (1996).

environments in which the hylobatids have evolved. Although traditionally thought of as territorial displays between rival family groups (Ellefson 1974), these duets probably also convey information about the strength of the pair bond (relationship) between the sexes as well as the health and physical condition of the individual partners (Haimoff 1984). Thus, it is significant that neither the larynx nor the vocal pitch of male and female gibbons is sexually dimorphic, a situation which contrasts markedly with that encountered in the orangutan and gorilla. The only known exception to this generalization concerns the white-cheeked gibbon (Nomascus concolor) in which the adult male possesses a small throat sac. Deputte (1982) described a low-pitched sound given by adult males, in association with air entering this vocal sac, and he says that 'this sound is a new acquisition in the mature, adult male vocal repertoire.' However, as Deputte notes, loud calls are given by both sexes in mated pairs of white-cheeked gibbons, so that the functional significance of the throat sac in adult males remains unclear. Among the twelve to fourteen species of gibbons currently recognized (Groves 2001; Bar-tlett 2007), absence of sexual dimorphism in body size, laryngeal structure, and vocal pitch appears to be the rule. However, detailed studies of vocal anatomy remain to be carried out for some gibbon species, so it is possible that sex differences remain to be described.

Can the principles derived from observations of the vocal displays and laryngeal anatomy of the apes be applied to the primates as a whole? Is the larynx or its extensions (vocal sacs) larger, and are loud calls more specialized, in males of polygynous monkey species? Are there consistent differences between polygynous species and those which have monogamous or multi-male/multi-female mating systems? Are the effects of sexual selection upon vocal tract anatomy greatest in forest-living monkeys, in which groups are spatially separated and, if so, are such effects most pronounced in species which form polygynous one-male units? In this regard it is instructive to consider the guenons (Genus Cercopithecus) and the colobine monkeys of

Africa and Asia, because species with polygynous and multi-male/multi-female mating systems are well represented in both these groups. Many of them are highly arboreal and inhabit rainforests. Gautier (1971; 1988) studied the loud calls of forest guenons in relation to the functions of the adult male's ventral (sub-hyoid) laryngeal sac. Adult males of species such as Cercopithecus mona, C. pogo-nius, C. neglectus, and C. nictitans have much larger vocal sacs than females and they emit distinctive resonant 'booms' as part of their loud call displays. These species all have predominantly polygynous mating systems. Gautier has shown that the male's laryngeal sac is filled with air prior to booming (Figure 8.7) and that making a fistula in the sac of C. neglectus markedly decreases sound production (Gautier 1971). These findings strengthen the conclusion that vocal sacs act in some way as resonators during loud calls. This is likely to be the case, for example, in the male orangutan, which can retain up to 6 litres of air in its vocal sacs (Starck and Schneider 1960). Some authorities have rejected the idea that laryngeal sacs evolved to enhance vocal

Frog Vocal Sac

Figure 8.7 Functions of the laryngeal sac during 'booming' vocalizations by an adult male De Brazza's monkey {Cercopithecus neglectus). 1-4: inflation of vocal sac accompanied by sound {spectra A, B); 5-7: emission of booming call {spectra C, D); 8: conclusion of call. Source: From Dixson {1998a); modified after Gautier {1971).

Figure 8.7 Functions of the laryngeal sac during 'booming' vocalizations by an adult male De Brazza's monkey {Cercopithecus neglectus). 1-4: inflation of vocal sac accompanied by sound {spectra A, B); 5-7: emission of booming call {spectra C, D); 8: conclusion of call. Source: From Dixson {1998a); modified after Gautier {1971).

displays (Negus 1949; Harrison 1995). Yet the bulk of the behavioural evidence supports the view that the laryngeal sacs act as resonators in various nonhuman primates, and that their greater size in adult males of some species is linked to the production of deeper, more resonant calls. In addition, Hewitt, MacLarnon, and Jones (2002) have proposed that the vocal sacs of the great apes and the siamang may also function to recycle exhaled air during fast call sequences, and to reduce the risk of hyperventilation during these displays.

In the leaf-eating monkeys (Subfamily Colobinae) of Africa and Asia, the larynx is sexually dimorphic in some species and once again this is associated with the emission of loud resonant calls by adult males. In the King colobus (Colobus polykomos) and the closely related mantled guereza (C. guereza), the larynx is especially large in mature males which produce loud roars during displays between polyg-ynous one-male units. Hill and Booth (1957) measured the laryngeal dimensions of the African King colobus, olive colobus, and red colobus, as well as five species of Asiatic leaf-eating monkeys. They noted that the male King colobus has by far the largest larynx and that its size is 'equal to that of an adult human male.' Given that an adult male King colobus weighs only 10 kg, the size of its larynx in relation to body size is truly remarkable. By contrast, the red colobus (Procolobus badius) and olive colobus (P. verus), both of which have multi-male/multi-female mating systems, lack the vocal power of the King colobus and have much smaller larynges. John Oates and his colleagues have argued that the distinctive roars of black and white colobus monkeys, which are best developed in C. guereza, are derived in evolution from an originally multi-male/multi-female call type, such as currently occurs in the black colobus (C. satanas). The male's call may have functioned originally as an alarm call, and then become modified for use in inter-male competition within the social group. Sexual selection may have favoured the evolution of a larger larynx in adult males under these conditions to produce calls of deeper pitch. Assumption of polygynous, singlemale social groupings in the King colobus and mantled guereza would have been associated with still greater sexual selection for laryngeal enlargement to enhance vocal capacity. All this is derived, however, from the possession of a small larynx in ancestral forms, as this is 'the presumed primitive condition for African colobines' (Oates, Bocian, and Terranova 2000).

Hill and Booth (1957) also noted the occurrence of an enlarged larynx in Asiatic leaf monkeys such as the lutongs (Trachypithecus), Gray langurs (Semno-pithecus), and the proboscis monkey (Nasalis). They comment that possession of a sub-hyoid laryngeal sac is associated with greater vocal resonance in these monkeys, many of which have polygynous mating systems. This is the case, for example, in the Northern plains gray langur of India (Semno-pithecus entellus), in which adult males emit loud 'whooping' calls during inter-group encounters. In a related species, S. johnii, only the leader male in a one-male unit calls in this fashion, whereas several males may call together in larger groups of S. entellus (Hohmann 1989). Hohmann also made the interesting observation that males inflate their vocal sacs during their whooping displays. However, one male whose sac had been punctured due to a bite wound was unable to emit whooping calls at full volume.

Loud calls are given by adult males in a number of Old World monkeys which live in multi-male/ multi-female social groups. Examples include the 'whoopgobble' calls of the forest-dwelling manga-beys (Lophocebus and Cercocebus) and the 'roar-grunts' of baboons (Papio). In his review of the evolution of these calls, Wasser (1982) points out that they tend to be of lowest frequency and most stereotyped in structure among forest-dwelling species. Individual males may be readily distinguishable by their loud calls, as is the case in the arboreal mangabeys. Thus the calls may play some role in communication between males within and between groups, under conditions where visual signaling is limited due to the dense vegetation. However, these calls are neither as loud, nor as resonant, as the loud calls of the polygynous guenons and black and white colobus monkeys described above. Nor is sexual dimorphism in laryngeal size and structure as marked in the mangabeys and baboons.

Among the New world primates, a substantial number of genera contain species which live in small family groups with pair-living (monogamous) mating systems. Examples include the owl monkeys (Aotus), titi monkeys (Callicebus), marmosets and tamarins (Family Callitrichidae), and the white-faced saki (Pithecia pithecia). Many of these monkeys emit long calls and members of a mated pair may synchronize their calls to produce duets. These function for territorial defence and group cohesion (e.g. in cotton-top tamarins, Saguinus oedipus: Snowdon and Soini 1988; pygmy marmosets, Cebuella pygmaea: Soini 1988, and Callicebus species: Kinzey 1981). In the golden lion tamarin (Leontop-ithecus rosalia), Kleiman, Hoage, and Green (1988) state that long calls 'serve to cement and maintain the pair bond but also to advertise presence in a territory.' Golden lion tamarins have a ventral laryn-geal air sac, but this is situated lower down in the larynx, rather than being sub-hyoid in position, as in colobines. Hershkovitz (1977) noted that this air sac was better developed in three adult males than in two adult females that he dissected. However, sex differences in vocal tract anatomy are not well represented among the monogamous New World primates as a whole. It appears that, like the gibbons, these pair-living New World monkeys accomplish their duets by means of laryngeal mechanisms which are the same, or at least very similar, in the two sexes. In the nocturnal owl monkeys (Aotus), males and females are both capable of giving very low frequency 'hoot calls', but these are emitted by individual monkeys and not as part of territorial duets. Both sexes also give a 'resonant whoop', rising in pitch and volume, as a prelude to aggression between family groups. Males and females inflate their throat sacs before uttering these calls (Moyni-han 1964; Wright 1994).

The most spectacular specializations of primate vocal tract anatomy concern the howler monkeys (Alouatta), which are widely distributed in the rainforests of Central and South America. Their social groups usually contain 'one or a small number of adult males and several adult females'.

Males are from 20 per cent to 50 per cent heavier than females, depending upon the species considered (Di Fiore and Campbell 2007). Howlers are famed for their loud, resonant roaring vocalizations, and for the remarkable development of the vocal apparatus and laryngeal sacs, especially in adult males. The hyoid bone at the base of the tongue is hollow and egg-shaped in adults of both sexes, but in males the bone is so large that it causes a marked swelling beneath the chin. The red howler (Alouatta seniculus) shows the most extreme sex differences in the size of its vocal apparatus (Figure 8.8) and it emits the most powerful calls. The volume of the male's hyoid is five times greater than that of the adult female, whereas in male mantled howlers (A. palliata) it is a little more than twice as large (Table 8.1).

The precise functions of the loud vocalizations of howlers have been much debated. Both sexes may vocalize, especially in the early morning, so that group choruses may play some role in inter-troop spacing (mantled howler: Carpenter 1965). However, Sekulic (1982) has shown that howlers often call at other times of day and that they roar in order to challenge solitary individuals outside the group, as well as neighbouring groups. She suggested that howlers assess and repel competitors by means of vocal displays, thus reducing the likelihood of energetically costly chases and fights. Competition occurs between males in reproductive contexts, and the sex differences in hyoid volume and vocal pitch are intriguing in this respect. In the red howler, genetic studies have shown that dominant males sire the majority of the offspring (Pope 1990). The pronounced development of the hyoid in male red howlers may relate to the importance of polygyny in its mating system. Thus in the red howler, and in several other species (e.g. A. caraya, A. guariba, and A. pigra), there is usually only one adult male in the social group (Di Fiore and Campbell 2007). However, in the mantled howler, which has the least sexually dimorphic vocal apparatus,

Table 8.1. Hyoid volumes and socionomic sex ratios in howler monkeys (Alouatta).

Socionomic

Hyoid volume (ml)

Species

sex ratio*

Male

Female

Female/Male %

A. palliata

2.63

4.5

2.0

44

A. seniculus

1.55

69.5

12.5

18

A. belzebul

2.0

56.5

12.5

22

A. fusca

-

39.0

8.5

22

A. caraya

1.73

23.0

8.0

35

*Socionomic sex ratio = nos. of adult females / nos. of adult males per group. Data from Crockett and Eisenberg, 1987; Di Fiore and Campbell, 2007, and after Dixson, 1998a.

*Socionomic sex ratio = nos. of adult females / nos. of adult males per group. Data from Crockett and Eisenberg, 1987; Di Fiore and Campbell, 2007, and after Dixson, 1998a.

Figure 8.8 The hyoid apparatus and associated anatomical specializations In an adult male howler monkey (Alouatta seniculus). 1. Processus furcatus; 2. lingula of cuneiform cartilage; 3. Arrow through thyrocuneiform space of left side; 4. lingula of epiglottic cartilage; 5. Cornu branchiale.

Source: From Dixson (1998a), after Schon (1971).

larger multi-male/multi-female social groups are more common.

One interpretation to be made on the basis of this brief overview of primate vocal anatomy and mating systems is that sexual selection has favoured the greatest development of laryngeal and associated specializations in adult males of species which are polygynous. Sex differences certainly occur in multi-male/multi-female species, but sexual dimorphism tends to be less pronounced under these conditions. By contrast, in most primates that live in small family groups, and which have principally monogamous mating systems, the anatomy of the vocal tract and pitch of calls produced are very similar in males and females. In order to quantify sex differences in the structure of the larynx, laryngeal sacs, and hyoid in relation to primate mating systems, I

have employed a rating scale, similar to that which was used in the last chapter to quantify sex differences in visual traits. This scale extends from zero (no sex differences in vocal tract anatomy), up to a maximum score of 5 (marked sexual dimorphism: adult males have a much larger larynx/vocal sacs/ hyoid). In the absence of precise anatomical measurements of both sexes across a wide range of primate species, the rating scale provides a useful way of facilitating statistical comparisons of sexual dimorphism in primates that are monogamous, polygynous, or that have multi-male/multi-female mating systems. It was possible to assign ratings to representatives of twenty-four anthropoid genera, including Homo. The results, shown in Figure 8.9, indicate that adult males of polygynous forms have consistently larger and more specialized vocal tracts

Polygyny Monogamy Multi-male / multi-female

Figure 8.9 Sexual dimorphism in the vocal apparatus (larynx, laryngeal sacs, and hyoid) and mating systems in primates. Data are ratings of the degree of sexual size dimorphism (male>female) in twenty-four primate genera, including Homo. ***P<.001. Further details are provided in the text.

Polygyny Monogamy Multi-male / multi-female

Figure 8.9 Sexual dimorphism in the vocal apparatus (larynx, laryngeal sacs, and hyoid) and mating systems in primates. Data are ratings of the degree of sexual size dimorphism (male>female) in twenty-four primate genera, including Homo. ***P<.001. Further details are provided in the text.

than adult females, and that their rating scores are significantly greater than either the multi-male/ multi-female or monogamous genera. Homo sapiens, with a markedly larger larynx in males, scores 3.5 on the rating scale, and thus falls among the polygynous primate genera. Multi-male/multi-female primate genera have average ratings of 2.35 for sexual dimorphism of the vocal tract, whereas in monogamous genera the mean score is 0.55.

These results are preliminary, as detailed studies will be required to obtain exact measurements of the vocal tracts of both sexes for a large enough sample of primates to facilitate a definitive test of the hypothesis. This will be a challenging task, however, due to the scarcity of suitable material for anatomical study. In the interim, the results presented here support the view that the larger larynx and deeper voice of the human male results from evolution by sexual selection, and that the emergence of this trait is likely to have occurred in ancestors of Homo sapiens which had polygynous mating systems. The ancestral forms concerned may have been very ancient indeed, perhaps as part of the australopithecine lineage that still lived in partially forested environments. It is probable that sex differences in vocal tract anatomy were well established early in human ancestry and prior to the emergence of language. In this regard, a fascinating discovery was made by Alemseged et al. (2006) during their restoration of the partial skeleton of a 3.3 million year juvenile specimen of Australopithecus afaren-sis. Amazingly, the hyoid bone has survived in this specimen, which is from the Dikika region of Ethiopia. The structure of the hyoid shows similarities to that of the gorilla and chimpanzee and 'almost certainly reflects the presence of laryngeal air sacs characteristic of African apes'.

Sex differences in human vocal pitch relate primarily to anatomical differences in the size of the larynx and vocal cord length in men and women, although there are also sex differences in functioning of the vocal tract above the level of the larynx

(Balaban 1994). The lateral laryngeal sacs, which are much enlarged in the great apes and in the siamang, are represented only by small pouches in human beings. All primates possess lateral laryngeal sacs, so that their occurrence in Homo sapiens is a primitive feature. Their small size may be due to reduction from larger structures in ape-like ancestors (e.g. in australopithecines), perhaps in association with changes in respiratory control which accompanied the evolution of language (Hewitt et al. 2002). On the other hand, it is possible to argue, and with equal justification, that the lateral laryngeal sacs may never have been especially large in human ancestors. Enlargement of the cartilages of the male larynx and lengthening of the vocal cords in Homo may have occurred independently of changes in the vocal sacs.

Previous chapters have emphasized that many features of the human reproductive system are consistent with an evolutionary ancestry involving polygyny or monogamy rather than a multi-male/multi-female mating system with its associated specializations for sperm competition and cryptic female choice. The sex differences in laryngeal structure and vocal pitch described here take us one step further in the quest to understand whether human ancestors had either monogamous or polygynous mating systems. Human sex differences in the anatomy and functions of the vocal tract are consistent with effects of sexual selection operating within a polygynous mating system, early in the evolutionary line which gave rise to human beings. Even now, in a modern hunter-gatherer population, the deeper voice of the human male correlates with traits which positively impact masculine reproductive success (Apicella et al. 2007). Thus, insights gained from comparative studies of the primate larynx support the conclusion reached in Chapter 7 that polygyny has played an important role in the ancestry of Homo sapiens.

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