Cryptic female choice: criteria for establishing female sperm choice.
The possibility that females might exert physiological control over the probability of fertilization by certain sperm has been discussed for many years (Tyler 1948; Bedford 1965; Cohen 1969; Lloyd 1979). Studies in which females are inseminated by males of a closely related species (heterospecific crosses) often result in reduced fertilization, strongly suggesting that females possess mechanisms to discriminate between sperm from hetero- and conspecific males (Dobzhansky 1951; Hewitt et al. 1989; Bella et al. 1992; Robinson et al. 1994). In some cases, the mechanism of heterospecific sterility is known: following heterospecific inseminations between certain Drosophila species oviposition is blocked, but can be stimulated by injecting females with the seminal fluid (but no sperm) of conspecific males (Fuyama 1983; reviewed in Markow 1997). These studies indicate that at an interspecific level the ability of females to discriminate between sperm is often well developed. Many fewer studies, however, have considered whether females have the ability to discriminate between the sperm of different conspecific males. Thornhill (1983, 1984) referred to any postcopulatory ability of females to favor one (conspecific) male over another as cryptic female choice, describing them as "cryptic" because these processes take place inside the female's body and cannot be observed directly. At that time, few behavioral ecologists attempted to test the idea of cryptic female choice. This is surprising given the number of studies that were then underway on precopulatory female choice (see Andersson 1994). There were two probable reasons for the apparent lack of interest. First, just as had occurred with precopulatory female choice, cryptic female choice was considered to be a less powerful and hence a less important selective force than sperm competition (e.g., Parker 1979, 1984). Second, the study of cryptic female choice required an understanding of the mechanisms associated with insemination, sperm storage, and fertilization, which were areas few evolutionary biologists were trained to explore. More recently, an interest in female perspectives (e.g., Lifjeld and Robertson 1992; Birkhead and Moller 1993; Hunter et al. 1993) and a rekindling of interest in mechanistic explanations for behavioral phenomena (e.g., Krebs and Davies 1997) has helped to bring cryptic female choice to the attention of biologists (Eberhard 1985, 1996). In addition, it is now clear that many male and female reproductive traits coevolve (Eberhard 1985; Rice 1996; Wiley 1997). Although this does not necessarily include cryptic female choice, the mechanisms of sperm utilization will undoubtedly influence sexual conflict and may play a role in the coevolution of male and female reproductive traits (Parker 1979; Stockley 1997a; Brown et al. 1997; Price 1997).
Females can potentially influence which males father their offspring before or after copulation. Precopulatory female choice is reasonably well established because females of many species appear to exert considerable influence over which males they copulate with (reviewed in Andersson 1994). Postcopulatory choice can occur either prior to or after fertilization. Postfertilization female choice can occur through the differential abortion of embryos (e.g., Hull 1964; Willson and Burley 1983) and/or differential investment in offspring (Willson and Burley 1983; Simmons 1987; Burley 1988).
The existence of postcopulatory prefertilization female sperm choice is more controversial, in part because, if it occurs, it does so at the same time as sperm competition. Distinguishing between these processes is extremely difficult. Eberhard (1996) has identified 20 different ways by which cryptic female choice may occur and has defined it thus: "Sexual selection by cryptic female choice can result from a female-controlled process or structure that selectively favors paternity by conspecific males with a particular trait over that of others that lack the trait when the female has copulated with both types" (Eberhard 1996, p. 7). As Simmons and Siva-Jothy (1998) have pointed out, postcopulatory prefertilization female choice can be either sequential or simultaneous. When choice is sequential, a female is inseminated by one male but ejects (or neutralizes) all or most of his sperm prior to copulating with another male. In this situation the sperm from different males are unlikely to coexist in the female reproductive tract, they cannot interact directly, and they cannot provide the female with an opportunity to discriminate between them. However, it is still feasible that females may discriminate between males or their sperm on this basis (Janetos 1980). The simultaneous occurrence of sperm from two (or more) males in the female tract is more likely to occur and provides the opportunity for females to choose between the sperm of different males (Simmons and Siva-Jothy 1998). The simultaneous recognition of and discrimination between sperm of different males, either on the basis of the males' phenotype or that of their sperm constitutes sperm choice and is the focus of this review.
In recent years several studies have claimed to provide evidence for sperm choice. For example, the observations that females of some species possess more than a single sperm storage structure or store sperm from different males in different parts of the reproductive tract have been taken as evidence for sperm choice (references in Eberhard 1996). Although these observations are consistent with the occurrence of sperm choice, they are not sufficient to demonstrate it. By overstating their claims, authors may mislead the scientific community to believe that sperm choice is a frequent occurrence when its existence has not been properly confirmed in any species. Only if we are aware of what does and does not constitute evidence for sperm choice can we be confidently identify its occurrence.
The criteria for cryptic female choice in general have been considered by Thornhill (1983, 1984) and Eberhard (1996, pp. 80-81) and are similar to those devised for precopulatory female choice when this was in dispute (Halliday 1983; Searcy and Andersson 1986; Heisler et al. 1987; Ryan and Keddy-Hector 1992; Andersson 1994; see also Eberhard 1996, p. 81). Although Eberhard (1996, p. 80) acknowledges that making a strong case for cryptic female choice is complex, he also asserts that cryptic female choice is widespread. In part this stems from the fact that his definition of cryptic female choice (above) is broad and explicitly includes some processes under female behavioral control (but not obviously cryptic). For example, the extent to which a female remates or oviposits after copulating with a particular male or how long she allows an external spermatophore to remain attached (e.g., Simmons 1986; Sakaluk and Eggert 1996) comprise instances of postcopulatory behavioral control by females. These cases appear to be well substantiated and are therefore not an issue. In my opinion the controversy in the field of cryptic female choice lies in whether sperm choice occurs. I describe the main criteria that must be met in order to demonstrate sperm choice by these means and reconsider a number of the examples that purport to show sperm choice in the light of these criteria.
When a female is inseminated by more than one male, the resulting paternity can be the consequence of any combination of: sperm competition, differential abortion, or female sperm choice. The existence of sperm competition as an important factor affecting paternity is well established (Parker 1984, 1998). Therefore, the most plausible way to demonstrate the occurrence of female sperm choice is to control for both differential abortion and sperm competition. In some species, at least, differential abortion can be accounted for by recording the proportion of undeveloped eggs sired by each male. Controlling for sperm-competition effects is more difficult but can be achieved in particular experimental designs. Sperm-competition experiments mainly have been conducted in two ways. First, in birds and mammals (in which artificial insemination is possible) females can be inseminated just once with a mixture of known numbers of sperm from each of two males (e.g. Martin et al. 1974; Dziuk 1996). This design avoids the complexity of insemination-order effects, which often occur when separate inseminations are made (Birkhead and Biggins 1998). Second, the classical sperm-competition study conducted on insects, other invertebrates, and birds comprises each of several females being inseminated sequentially by a pair of males in a reciprocal design such that in half the cases the sperm of one male is inseminated first and in the other half, second (Boorman and Parker 1976; Birkhead and Biggins 1998). The proportion of offspring fathered by the first and second male are referred to as [P.sub.1] and [P.sub.2], respectively (Boorman and Parker 1976). Because in many taxa, especially insects and birds (Birkhead and Parker 1997), the second or last insemination fertilizes the majority of eggs, the outcome of sperm-competition experiments are often expressed in terms of [P.sub.2]. Intermediate values of [P.sub.2] are usually indicative of sperm mixing and random utilization, whereas high values of [P.sub.2] indicate nonrandom utilization of sperm (Simmons and Siva-Jothy 1998). The reciprocal experimental design allows one to establish whether order effects are symmetrical for each male in a pair (Boorman and Parker 1976). Until recently the results of most sperm-competition studies were presented as mean [P.sub.2] values. However, Lewis and Austad (1990) drew attention to the considerable variance that exists around [P.sub.2] values in such studies and identified a way in which some of this variance could be attributed to differences between either males or females. In their study of Tribolium castaneum they allowed 11 male pairs to copulate in the same sequence eight times, each time with a different virgin female. Using ANOVA, they showed that [P.sub.2] values were significantly repeatable for particular male pairs and that 17.8% of the variance in [P.sub.2] was attributable to differences among male pairs. They also showed that after accounting for this male effect, there was a large error variance (among females and within males; 57.7%), which encompassed several sources of variation, including the differential use of sperm by females.
The design of Lewis and Austad's (1990) study provides a useful general approach for identifying the criteria necessary to demonstrate female choice of sperm. It may also be possible to demonstrate female sperm choice using other methods, as in the unusual instance of Beroe in which female sperm choice can be observed directly (see below). In standard sperm-competition experiments like those described above, three criteria must be met to demonstrate female sperm choice. There must be variance in [P.sub.2] (or, in the case of a single mixed insemination, variance the proportion of offspring fathered by one of the males), and some of this variance must be attributable to both females and males. Attributing variance to males will usually comprise attributing variance to a pair of males, as in Lewis and Austad's (1990) study, although more complex experimental designs could attribute variance to individual males. This, however, is beyond the scope of the present paper.
By employing an experimental design in which the same pairs of males inseminate several different females or the same females are inseminated by the several pairs of males (for example, over different breeding cycles), it should be possible to attribute some of the variance in [P.sub.2] to males or females. For example, imagine an experiment like that of Lewis and Austad's (1990) in which several pairs of males each inseminate a number of different females. Repeatability (Falconer 1981; Lessells and Boag 1987) in [P.sub.2] values among females inseminated by the same pair of males would constitute good evidence that some of the variance in [P.sub.2] was attributable to male pairs. Although it is also possible in an experimental design like that of Lewis and Austad's (1990) to estimate the variance in [P.sub.2] between females and within males, which includes the possibility of female sperm choice, estimating the proportion of variance attributable to females more precisely requires another experiment. This additional experiment comprises several females each inseminated by several different pairs of males in successive breeding cycles. If individual females show significant repeatability in [P.sub.2] values this would be good evidence that females were responsible for some of the overall variance in [P.sub.2]. It might be assumed that to demonstrate female sperm choice only the second experiment is necessary. However, to identify the differences between males (or their sperm) that account for female sperm choice it is also necessary to be able to attribute variance in [P.sub.2] to males, so both experiments are required.
The examples presented here were selected for two reasons: (1) in all cases the authors have strongly asserted the existence of cryptic female choice, specifically, sperm choice; and (2) the studies vary considerably in the quality of evidence used to support the claim of sperm choice. This is not a comprehensive review - this has already been provided by Eberhard (1996): however, my criteria for accepting the existence of sperm choice are more stringent than those of Eberhard (1996). My aim is to illustrate the difficulty of demonstrating sperm choice and to establish to what extent the three criteria above have been met.
Baker and Bellis (1995) have asserted that cryptic female choice is important in humans. They propose that females control the paternity of their offspring through the differential retention of sperm. They reported that females ejected fewer sperm following copulations in which they experienced orgasm close to the time of male ejaculation than following copulations in which they did not experience orgasm (Baker and Bellis 1995, pp. 234-236). Although this is consistent with female sperm choice, because none of the criteria in Table 1 are met it does not constitute evidence for sperm choice.
Chrysomelid Beetle, Chelymorpha alternans
The male of this beetle is unusual in having an extremely long flagellum associated with its penis (V. Rodriguez, cited in Eberhard 1996, p. 6). During copulation the flagellum is threaded up the female's long and convoluted spermathecal duct and into the ampulla and occasionally also into the spermatheca. The male deposits a spermatophore in the female's bursa, and sperm migrate along the flagellum up the spermathecal duct to the spermatheca. In sperm-competition experiments involving two or three males, the proportion of offspring sired by each male was correlated with the length of his flagellum (Eberhard 1996, p. 351). Eberhard (1996, p. 353) suggests that sperm dumping by females may be the mechanism responsible for this differential success. A higher proportion of females ejected a drop of sperm when they copulated with a male whose flagellum had been experimentally shortened (87.5%) than when they copulated with control males (13.1%; see also Dickinson 1997, p. 177-178). Eberhard (1996, p. 6) interpreted this as evidence for the preferential use by females of sperm from males with longer flagella. However, there are alternative explanations: males with a longer flagellum may simply be more efficient at getting their sperm to the best place to achieve fertilization and/or [TABULAR DATA FOR TABLE 1 OMITTED] they may inseminate more sperm (see also Dickinson 1997: Simmons and Siva-Jothy 1998). In summary, the data imply variance in [P.sub.2] and suggest that both the female and male have some influence over paternity (Table 1).
Yellow Dungfly, Scatophaga stercoraria
In sperm-competition experiments involving two male yellow dungflies, variance in [P.sub.2] occurs (Parker and Simmons 1994). After allowing female dungflies to copulate for a fixed time with two different males, Ward (1993) found that regardless of copulation order: (1) females stored more sperm from large than small males; (2) sperm from the two males were distributed nonrandomly across the female's three spermathecae; and (3) the larger male fertilized more eggs (see also Otronen et al. 1997; Ward 1998). Ward (1993) considered his results as evidence that females preferentially used sperm from large males. However, Simmons et al. (1996) challenged this interpretation and showed by another empirical study of Scatophaga that Ward's results could be equally or better explained by differential sperm displacement rates: when larger males copulated second they displaced previously stored sperm more rapidly than smaller males. Simmons et al. (1996) suggested that this is largely a consequence of larger males having larger sperm ducts that allow a faster flow of sperm (see Table 1). When larger males copulated first, they released more sperm, fewer of which were displaced by the second, smaller male.
Ascidians and Flowering Plants
Nonrandom utilization of sperm has been clearly documented in the ascidian, Diplosoma listerianum, a sessile, colonial, clonal, marine filter-feeder (Bishop 1996; Bishop et al. 1996). Diplosoma is a hermaphrodite and releases sperm into the water, from where sperm are taken up into the oviduct of a potential partner and fertilization occurs. However, if an individual takes up sperm from its own clone, the sperm do not progress any further than the anterior half of the oviduct. This suggests an antagonistic interaction between the sperm and the oviduct that serves as a block to selfing. The block is not perfect, however, and occasionally (in isolated colonies) selfing does occur, but cell division in the zygote is abnormal and embryos are always aborted (J. D. D. Bishop, pers. comm.). In addition, sperm from different clones are sometimes also blocked in the anterior portion of the oviduct, apparently due to incompatibility between clones (Bishop 1996; Bishop et al. 1996). Because of its biology, Diplosoma is not directly comparable with the other organisms in Table 1. It is difficult therefore to determine whether Diplosoma fulfills the criteria in Table 1, but there is some evidence that all are met. However, the case of Diplosoma raises the issue of whether this type of female preference for unrelated sperm constitutes classical, directional sexual selection (Darwin 1871). This issue is considered further below (Discussion).
A very similar effect of relatedness on female pollen choice also occurs in flowering plants (reviewed in Willson and Burley 1983; Delph and Havens 1998). Postpollination female choice via the effect of the stigma pollen-tube growth is well documented: incompatible combinations (e.g., self) result in reduced or nongrowth of the pollen tube. Moreover, pollentube growth has been shown, at least in some species, to require genetic compatibility between the pollen and the female tissue. In addition, several studies have shown a positive correlation between degree of pollen competition and offspring vigor, so that discriminating between the pollen from different males enhances female fitness (Willson and Burley 1983; Delph and Havens 1998).
One of the most intriguing examples of what might constitute sperm choice occurs in the ctenophore Beroe ovata (Carre and Sardet 1984; Carre et al. 1991). This study is unique in that female sperm choice can be observed directly. Examination of the transparent eggs of Beroe revealed that several sperm typically penetrate the ovum (polyspermy) and that the female pronucleus then moves around within the ovum to each of the male pronuclei in turn before fusing with one of them. The authors state that the behavior of the female pronucleus looks like mate choice. Other than knowing that the female pronucleus has an active role in fertilization and that this "choice" is not to avoid selfing (the block to selfing occurs at the egg envelope; Carre et al. 1991), there is no other relevant information (Table 1).
In the sand lizard, Lacerta agilis, females routinely and indiscriminately copulate with several males. Further, females that copulate with several males exhibit greater hatching success, lower incidence of deformities among offspring, and enhanced survival of free-living offspring as compared with females that copulate with only a single male (Olsson et al. 1994, 1996). Sperm-competition experiments in which females were inseminated by two males revealed that the male genetically more similar to the female (estimated via DNA fingerprinting) sired fewer offspring. Arranged matings confirmed that those between relatives produced fewer offspring. It was concluded that following inseminations by two males, females differentially use the sperm from the less-related male. Male effects were minimized (but not rigorously controlled) by taking into account numbers of sperm (albeit indirectly, via male size and hence testes mass) and time since the last ejaculation. Neither of these factors explained any of the variance in male fertilization success, thus reinforcing the conclusion that sperm choice occurs. The results could also be explained by differential zygote mortality, but a subsequent analysis (Olsson et al. 1997) showed that this was not the case. Although the study by Olsson et al. (1996) did not establish whether there was repeatability of [P.sub.2] effects across either male or females, this study provides some of the best evidence to date for sperm choice (Table 1).
Similar, although less comprehensive, results were obtained by Madsen et al. (1992) in another reptile, the adder Viperus berus: females copulated indiscriminately with several males, and the more partners a female had, the lower the level of mortality and morphological abnormalities in her offspring. Madsen et al. (1992) suggested that this occurred because the quality of males or their sperm differed, and multiple mating by females ensured that they were fertilized by the best-quality sperm.
Both Madsen et al.'s (1992) population of adders and Olsson et al.'s (1996) population of sand lizards are small and isolated with a relatively high degree of inbreeding. A study of a less-isolated population of adders found that a much smaller proportion of females copulated with more than one male and that those that did failed to show any greater offspring viability (Capula and Luiselli 1994). This suggests that the results of Madsen et al. and Olsson et al. may have been a consequence of their inbred study populations, and that female adders may copulate with multiple partners mainly when it is advantageous to do so.
Cowpea Weevil, Callosobruchus maculatus
Wilson et al. (1997) used an experimental design that was similar to but somewhat more elaborate than Lewis and Austad's (1990) in their study of paternity in Callosobruchus maculatus. Eady (1994) had previously shown that when two male C. maculatus copulated with a single female, [P.sub.2] values varied between zero and one. Wilson et al. (1997) then designed an experiment to determine how much of the variance in [P.sub.2] was attributable to females after controlling for male effects. This was achieved by comparing the repeatability of [P.sub.2] when the same two males copulated with three unrelated females and with three full sisters. The repeatability of [P.sub.2] was relatively low (r = 0.05-0.55) and nonsignificant with unrelated females, but it was both higher (r = 0.82-0.90) and significant between sisters, indicating a strong female effect and that female sperm choice has a genetic basis (Table 1). Wilson et al. (1997) also observed repeatability of male effects in one of their two experiments. Therefore, this study fulfills all three criteria in Table 1. However, Wilson et al. (1997) were unable to identify any male characters on which females might base their choice of sperm, and suggest that fertilization success in this species is a consequence of gamete compatibility or sperm-female compatibility.
This review raises two fundamental questions: Does sperm choice exist, and, if it exists, does it lead to sexual selection?
The evidence for sperm choice remains limited and few published studies fulfil all the necessary criteria (Table 1). In addition, some carefully conducted studies have found no evidence for sperm choice (Cunningham 1997; Stockley 1997b). The most important result to emerge from this review is that the few studies in Table 1 that provide evidence for sperm choice indicate not that sperm choice favors generally attractive males or their sperm, but that the selective basis for sperm choice favors sperm of particular genotypes to avoid selfing or other incompatible genetic combinations. This is consistent with the hypothesis that female organisms minimize the risk of a genetically incompatible partner by accepting sperm or pollen from several different males followed by the differential utilization of these gametes or differential abortion of zygotes made up of incompatible genotypes (Willson and Burley 1983; Zeh and Zeh 1996, 1997). There is abundant evidence that different individuals may be genetically incompatible, and that failure to avoid such combinations can reduce the fitness of both partners (Zimmering and Fowler 1968; Bateson, 1983). Incompatibility may arise from partners that are either genetically too similar or too dissimilar from one's self (Bateson 1983; Thornhill, 1993). For example, in Drosophila mojavensis following one generation of sib mating, females inseminated by a brother usually failed to lay any eggs, despite possessing an abundant supply of motile sperm (Markow 1982). This suggests that, just as in some heterospecific Drosophila studies (above), female D. mojavensis are able to differentially transport and utilize sperm from males of different relatedness. Sperm choice may be the most appropriate form of female choice in at least three situations. First, where females are unable to exert any precopulatory choice, which occurs when they are forcibly inseminated (Birkhead and Parker 1997). Second, if individuals do not have behavioral mechanisms for selecting a compatible partner, especially if their life-history features are such that the probability of being inseminated by a relative (or other inappropriate male) is high (e.g., Olsson et al. 1996; Markow 1997). Third, in sessile organisms, such as ascidians and plants, there can be no behavioral choice of male gametes; therefore, sperm choice and the postfertilization process of differential abortion may be especially important (Wirtz 1997) and may explain the more obvious nature of these forms of female choice in these taxa (Table 1).
Eberhard (1996) argued that cryptic female choice may be a much underestimated force in sexual selection. For cryptic female choice or sperm choice to be important components of sexual selection, these processes must enhance the fitness of females some way, either via Fisherian processes or via good genes. However, demonstrating enhanced fitness of females resulting from any form of female choice is extremely difficult. Indeed, in discussing precopulatory female choice Maynard Smith (1987) suggested that because female benefits are difficult to establish, they should not be part of the working definition of female choice. I have followed the same reasoning in this review and not included the demonstration of female benefits among the criteria for establishing female sperm choice. Nonetheless, some studies (e.g., Olsson et al. 1996) provide good evidence for enhanced female fitness resulting from what appears to be sperm choice. However, if (as this and several of the studies cited here indicate) it transpires that the main basis for sperm choice is the avoidance of incompatible male genotypes, then sexual selection via sperm choice will be relatively weak. The main reason for this is that females will be inconsistent in their choice: What is disadvantageous for one female may well be advantageous for another. Sperm choice will therefore create little skew in male mating success and hence will not constitute an important directional force in sexual selection. However, incest avoidance could potentially lead to enhancement in male phenotypes that promote courtship among unrelated individuals.
To answer the question of whether sperm choice occurs, I recommend that we design experiments that enable us to meet the criteria listed above. If we can satisfy ourselves that sperm choice occurs, we need then to identify the selection pressures that have favored its evolution. That is, we need to distinguish between cases that comprise sexual selection for generally attractive males or attractive sperm and the avoidance of genetic incompatibility. We also need to identify the physiological processes that allow females to recognize and differentially utilize sperm from different males.
I am extremely grateful to all those with whom I have discussed the issue of cryptic female choice and sperm choice and who took the time to answer questions, provide unpublished data, and read various drafts of the manuscript: A. P. Balmford, J. D. D. Bishop, H. Cronin, E. J. A. Cunningham, J. Dickinson, P. Lady, W. G. Eberhard, B. J. Hatchwell, E. Ketterson, A. P. Moller, M. Olsson, G. A. Parker, M. Petrie, S. Pitnick, F.L.W. Ratnieks, L. W. Simmons, M. T. Siva-Jothy, E. Tuttle, P. Ward, and J. Zeh.
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