Sperm number

Make Him a Monogamy Junkie

The Monogamy Method

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Theory predicts that an increased number of sperm is advantageous in sperm competition, either because a larger ejaculate volume displaces more rival sperm or due to numerical superiority. In general, sperm competition favouring numerous sperm may have led to the evolution of many tiny sperm and may even be responsible for the evolution of the two sexes (Parker et al., 1972; Bulmer and Parker, 2002). Comparative data in numerous animal groups have corroborated this finding. Males invest more resources in testes and sperm production when they encounter a greater risk of sperm competition (Smith, 1984; Birkhead and M0ller, 1998; Simmons, 2001). The same is found in butterflies. In species where females mate more frequently, as determined by spermatophore counts in wild-caught females, males have relatively larger testes (Gage, 1994). As yet, we do not know whether these males also produce more sperm. However, it seems likely, as in other insects, that there is generally a positive relationship between testis size and sperm number (Simmons, 2001). According to theory, we therefore expect that male butterflies and moths should increase the number of sperm when the risk of sperm competition is higher.

In general, we expect that in polyandrous species males should ensure that they are able to mate whenever they encounter a receptive female. In the polyandrous Australian Hypolimnas bolina butterfly, females show a facultative adult diapause, possibly due to the unpredictable timing of the tropical season. In contrast, males do not appear to be reproductively dormant, as sperm is present throughout the year. This may be a strategy to cope with the unpredictability of female activity and enable them to mate whenever they encounter receptive females (Pieloor and Seymour, 2001). In highly polyandrous species we also expect males to be able to produce more ejaculates than males of monandrous species, since they, on average, will mate more frequently. This is indeed the case; in butterflies, not only do males of polyandrous species produce bigger spermatophores than males of monandrous species (Svard and Wiklund, 1989; Bissoondath and Wiklund, 1995), they also have greater spermatophore production capacity. They are capable of producing new spermatophores and remating sooner than males of monogamous species (Svard and Wiklund, 1989).

3.3.1 Developmental response

One way in which larval experiences may influence adult mating strategy is through the presence of conspecific larvae. The number of conspecifics present may predict the eventual adult density. This in turn is likely to be related to the risk of sperm competition. The armyworm Pseudaletia separata has two larval phenotypes depending on rearing densities, a black-coloured gregarious 'crowded' type and a fast growing, pale green 'solitary' type. When armyworm outbreaks occur in the field, the density of adults becomes high and the crowded form is likely to be exposed to a higher risk of sperm competition. Accordingly, crowded type adults produce larger spermatophores (He and Tsubaki, 1992) with more apyrene sperm (He and Miyata, 1997) than those of the solitary type. This increase in apyrene number in the crowded type supports the hypothesis that apyrene sperm play a role in sperm competition, either by actively disrupting or displacing rival sperm or by influencing female sexual receptivity (He and Miyata, 1997). Females receiving spermatophores from males reared under crowded conditions delay remating for longer than females mated to males reared under lower densities (He and Tsubaki, 1995).

In Plodia interpunctella, larvae do not have distinct phenotypes depending on rearing density but exhibit a plastic response to variation in rearing density (Gage, 1995). Larval population structure influences adult population structure since, in this species, dispersal appears weak. In turn, adult population structure influences female mating pattern: females are more polyandrous at higher population densities. Males emerging into more dense populations therefore experience a greater risk of sperm competition and mate encounter. Accordingly, males reared at higher larval densities have larger abdomens, relatively bigger testes, and produce ejaculates containing more eupyrene and apyrene sperm. In contrast, males from lower densities have smaller testes and ejaculates but have relatively bigger thoraxes and heads and live longer as adults. These males appear to bias their reproductive strategy towards migration and mate searching. Such plasticity in reproductive strategy is likely to be particularly important for many lepidopteran species because adults are semelparous, short-lived and virtually all resources for reproduction are accrued in the larval stages.

Other species have evolved a fixed strategy to maximize their fertilization success that depends on the risk of sperm competition. In the polyandrous small white butterfly, Pieris rapae, the males' second spermatophores are only half the size of their first, but contain almost twice the number of apyrene and eupyrene sperm (Cook and Wedell, 1996). Even males remating on the same day as their first transfer increased the number of sperm on their second mating (Wedell and Cook, 1999a). Why do males have such different strategies on their first and second matings? Cook and Wedell (1996) hypothesized that the pattern of spermatophore allocation can be explained if males are more likely to encounter virgin females when mating for the first time. This seems likely, as there are two to three discrete generations of P. rapae per year (Asher et al., 2001), and adults are likely to emerge at similar times. With virgin females, males have complete confidence of paternity, and provide a large nutritious spermatophore to delay female remating and invest in offspring. On males' second matings, encountered females are likely to be non-virgin and males therefore have to compete with sperm from rival males. Males benefit by providing these females with high numbers of sperm, which leads to success in the resulting sperm competition, and reduced nutrient contribution, since they have lower paternity (Wedell and Cook, 1998).

In some species, males transfer an increased number of sperm on their second mating, even when remating on the same day, suggesting that males have a mechanism for reserving sperm for subsequent matings. Male butterflies and moths have a sperm storage organ, the duplex, in which sperm is retained after a mating in some polyandrous species. Male Lepidoptera eclose with a complete complement of sperm (Friedländer, 1997). Sperm release from the testes follows a daily rhythmic pattern and is controlled both by an intrinsic circadian mechanism present in the reproductive tract (Bebas et al., 2001), in combination with photoperiod and temperature (Riemann et al., 1974; Giebultowicz et al., 1989; Proshold, 1997). This results in an increased number of sperm available in the duplex as the number of days until mating increases (LaChance et al., 1977; Proshold, 1991; Giebultowicz and Zdarek, 1996). Males of polyandrous species do not necessarily ejaculate all the sperm they have stored in the duplex in a single mating (Hiroyoshi, 1995; Proshold and Bernon, 1994; Spurgeon et al., 1994; Wedell and Cook, 1999b; Seth et al., 2002b). This may be an adaptation by males to maintain sufficient sperm for additional matings, ensuring that high sperm numbers are available for their second mating, even if it occurs shortly after their first mating. Interestingly, the ability to retain sperm in the duplex varies between species and appears to be associated with variation in degree of polyandry. In the polyandrous P. napi and P. rapae, males reserve sperm in the duplex (N. Wedell and PA. Cook, unpublished data) and increase the number of sperm provided to females even when remating only 1 hour after their first copulation. In contrast, the monogamous brimstone males ejaculate all available sperm from the duplex (N. Wedell and PA. Cook, unpublished data), and require several days before being able to produce a new spermatophore, which can result in a female remaining in copula for up to a week if she has the misfortune to encounter a recently mated male (Labitte, 1919).

3.3.2 Ejaculate tailoring

Individual males can strategically ejaculate their limited sperm to maximize their fertilization returns. There is evidence that males assess sperm competition risks at a given mating and respond by increased ejaculate expenditure when risks are elevated. However, spermatogenesis is far from limitless, and males have evolved mechanisms for allocating their finite numbers of sperm optimally to maximize their lifetime reproductive success (Wedell et al., 2002b). Accordingly, males are expected to vary the number of sperm in relation to risk of sperm competition and female fecundity. Males appear to be able to assess mating status and the relative fecundity of females, and to modulate their ejaculate investment (Wedell et al., 2002b). Female reproductive 'quality' may be an important parameter that males have evolved sensitivity to. Female quality can arise from potential fecundity (e.g. body size or age) or female mated status (e.g. risk of sperm competition). When female reproductive quality varies and males are sperm-limited, selection may operate upon males to discriminate between female partners. Indeed, there is some behavioural evidence for male mate choice in butterflies (e.g. in the orange tip butterfly Anthocaris cardamines; Wiklund and Forsberg, 1985; and possibly in Acrea encedon; Jiggins et al., 2002). However, fewer studies have examined discrimination at the level of the gamete.

fecundity. In Plodia interpunctella, female potential fecundity is dictated by adult body size: heavier females have larger ovaries and live longer as adults

(Gage, 1998). Although male body weight does not constrain his first spermatophore size, males are sensitive to female weight and allocate more sperm to heavier females (Gage, 1998). Males may allocate more sperm to heavier females because of greater potential fecundity. They do not ejaculate larger spermatophores into bigger females because they have larger copulatory bursae: bursal size is not related to body size. However, heavier females do have larger spermathecal volumes. In addition, larger females are also more polyandrous than smaller females (perhaps linked to variance in spermathecal volume). Males may therefore also ejaculate more sperm into larger females because of the increased risk of sperm competition associated with such matings. In the gypsy moth, Lymantria dispar, males are sensitive to variation in female age and provide older females with less sperm than younger ones (Proshold, 1996). Older females may provide lower fecundity returns and also generate higher risks of sperm competition.

mating status. When detectable, female mated status predicts the risk of sperm competition that a male's ejaculate will subsequently face, and hence we expect males to provide more sperm to mated females. In the Indian meal moth, for example, males provide more sperm to non-virgin females (Cook and Gage, 1995). The small white butterfly, Pieris rapae, provides a striking suggestion that males indeed tailor the number of sperm provided in relation to risk of sperm competition. In this species, males are not only sensitive to the mating status of the female, and provide more sperm to mated females, but also to the mating status of the female's previous mate. This directly translates to varying sperm competition risk. In this species, mated males provide more sperm than virgin males; hence, when a male mates with a female previously inseminated by a mated male he will have to compete with more sperm than a male mating with a female inseminated with a virgin male. Amazingly, males vary the number of sperm and provide more sperm when the female has previously mated with a mated than a virgin male (Wedell and Cook, 1999a). It is possible that males can assess the mating status, and therefore the number of sperm they will compete with during mating, as remnants of males' spermatophores remain within the female's bursa, where males construct the spermatophore during copulation, and mated males produce smaller spermatophores than do virgin males.

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