The mammalian oviduct sperm competition and cryptic female choice

It is of the greatest interest, given that hundreds of millions of spermatozoa are deposited in the vagina at ejaculation, that only a few hundreds or thousands of these gametes are recoverable from the oviduct. In Table 4.2, examples are provided of numbers of sperm deposited during copulation, and numbers recovered from the oviducts of various mammals, including Homo sapiens. These numbers do not represent the only spermatozoa to reach the oviducts. Rather they constitute 'snapshot' counts of a small, transient population of sperm which pass through the oviduct, and which are replenished by gametes moving upwards through the uterus and uterotubal junction, to enter the isthmus (Figure 4.4). In the isthmus, spermatozoa typically adhere for a time to the oviductal epithelium before migrating to the upper part of the oviduct (ampulla) where fertilization takes place (Harper 1994; Yanagimachi 1994). This transitory association between spermatozoa and the isthmic epithelium is of great importance for fertility. A temporary pool of gametes is created, in which spermatozoa may accumulate until ovulation occurs and ova are transported to the ampulla (Figure 4.4). During their sojourn in the isthmus, spermatozoa may complete the changes (capacitation) required to enable them to move rapidly through the oviduct (hyperactivated motility) and penetrate the egg and its vestments (Yanagimachi 1994).

Table 4.2 Numbers of spermatozoa ejaculated, sites of deposition, and numbers of sperm arriving in the oviduct in mammals

No. of spermatozoa Site of sperm Sperm nos. in

Table 4.2 Numbers of spermatozoa ejaculated, sites of deposition, and numbers of sperm arriving in the oviduct in mammals

No. of spermatozoa Site of sperm Sperm nos. in

Species

per ejaculate

deposition

ampulla

Human

280 million

Vagina

200

Mouse

50 million

Uterus

<100

Rat

58 million

Vagina

500

Rabbit

280 million

Vagina

250-500

Ferret

Uterus

18-1600

Guinea pig

80 million

Vagina and

25-50

uterus

Domestic cattle

3000 million

Vagina

A few

Sheep

1000 million

Vagina

600-700

Pig

8000 million

Uterus

1000

Source: Data from Harper (1994); after Dixson (1998a).

Source: Data from Harper (1994); after Dixson (1998a).

Uterotubal Uterine cavity junction

Fundus of uterus

Isthmus of oviduct (thousands of sperm)

Ampulla (hundreds of sperm)

Uterotubal Uterine cavity junction

Fundus of uterus

Isthmus of oviduct (thousands of sperm)

Ampulla (hundreds of sperm)

Fimbriae

External cervical os

> 200 Million sperm enter the vagina at ejaculation

Figure 4.4 The human female reproductive tract and post-coital sperm numbers recorded at various levels within the tract.

External cervical os

> 200 Million sperm enter the vagina at ejaculation

Fimbriae

Figure 4.4 The human female reproductive tract and post-coital sperm numbers recorded at various levels within the tract.

For those mammals in which females mate with multiple partners during the fertile period, it is not known to what degree the spermatozoa of rival males are represented in the oviductal populations listed in Table 4.2. It would clearly be valuable to know if all the males that mate with one given female contribute gametes to this oviductal sperm population and, if so, in what proportions their gametes are represented. In fruit flies (Drosophila) elegant techniques have been developed to label and identify the sperm of rival males, and to verify a last male advantage in siring offspring (Civetta 1999). In mammals, sperm competition is thought to represent a 'raffle' in which males allocating the greatest numbers of sperm are likely to experience an advantage in sperm competition, irrespective of the order of mating (Parker 1998). Thus it has been established that single litters of offspring may have multiple sires, as, for example, in Beld-ing's ground squirrel (Hanken and Sherman 1981), the common shrew (Stockley et al. 1993), the black bear (Schenck and Kovacs 1995), the Ethiopian Wolf (Sillero-Zubiri, Gottelli, and MacDonald 1996), and the cheetah (Gottelli et al. 2007).

Given the importance of sperm competition, might the oviductal environment filter the gametes of rival males in some way, so that some sperm secure an advantage over others in gaining access to ova? If so, are there structural differences between the oviducts of those mammals which commonly engage in sperm competition, and those which are monogamous or polygynous? In this regard, it is noteworthy that mammalian oviducts exhibit great differences in morphology, including their length (Hunter 1988). Some mammals have relatively long and convoluted oviducts, whereas in others the ducts are quite short. There are differences also in the morphology of the ciliated fimbria (which guide the ova into the entrance of the oviduct) as well as in internal features such as the structure of the uterotubal junction (Hunter 1988; Harper 1994). Some interspecific differences in oviductal morphology are illustrated in Figure 4.5, which includes Homo sapiens. The human oviduct is approximately 8-15 cm long (its average length is 11 cm) in its extra-uterine extent, whilst the intramural portion embedded in the wall of the uterus is about 1.5-2.0 cm long (Lisa, Gioia, and Rubin 1954; Pauerstein and Eddy 1979). In 1993, Gomendio

Guinea pig

Rabbit

Figure 4.5 Examples of oviductal morphologies in mammals, to illustrate differences in the length and degree of coiling of the Fallopian tubes. The arrows indicate the approximate position of the junction between the isthmus and ampulla. Source: From Harper (1982).

Guinea pig

Rabbit

Figure 4.5 Examples of oviductal morphologies in mammals, to illustrate differences in the length and degree of coiling of the Fallopian tubes. The arrows indicate the approximate position of the junction between the isthmus and ampulla. Source: From Harper (1982).

and Roldan made the important discovery that sperm numbers in the ejaculates of eleven species of mammals (including H. sapiens) are positively correlated with oviductal lengths (after controlling for the effects of body size). The small sample sizes available to these authors restricted further work, but subsequently Gomendio et al. (1998) pointed out that 'it would make sense if polyandrous females had longer, more convoluted oviducts, so that sperm had to actively swim greater distances, and thus selection against less vigorous sperm could be more intense.' Anderson, Nyholt, and Dixson (2006) addressed this question by measuring oviduct length in a substantial sample of mammals (forty-eight species, representing thirty-three genera) and comparing residuals of oviduct length to residuals of testes size and sperm midpiece volumes in adult males of the same species. Multiple regression analyses showed that oviduct length correlates with testes size and sperm midpiece volume after controlling for effects of body size. The sample included mainly artiodactyls, carnivores, primates, and marsupials, and appropriate statistics were used to control for possible phylogenetic biases in the data set. Some results are shown in Figure 4.6 and data for H. sapiens have been included for comparative purposes. The human oviduct is relatively short, in relation to female body weight, and in relation to relative testes size and sperm midpiece volume in men.

A longer and more convoluted oviduct represents an additional challenge to sperm as they ascend the duct in order to fertilize the ova, either in the ampulla or at the ampullary-isthmic junction. When the sperm of rival males are present, an elongated oviduct may aid the female in selecting gametes of males with the greatest reproductive potential. It is the female's anatomy and physiology which challenges sperm in these ways; hence elongation of the oviduct in mammals where sperm competition is most likely may represent an example of sexual selection by cryptic female choice. The relatively short oviduct in H. sapiens is indicative of an evolutionary history involving low selection pressures for genital specialization and accords with the low values for relative testes size and sperm midpiece volumes in human beings.

Figure 4.6 Correlation between oviductal length and relative testes size in mammals. Data for Homo sapiens (•) are included for comparative purposes.

Residual testes size

Figure 4.6 Correlation between oviductal length and relative testes size in mammals. Data for Homo sapiens (•) are included for comparative purposes.

Source: Adapted from Anderson, Dixson, and Dixson (2006).

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