Evidence for a cost of sex in the freshwater snail Potamopyrgus antipodarum.
In a panmictic population with separate sexes, individuals will be under strong selection to invest equally in male and female offspring (Fisher 1930). When the sexes are equally expensive to produce, such selection will result in a 1:1 sex ratio. However, because males in such a population do not give birth to any offspring, the population is subject to invasion and replacement by clonal individuals that produce only female offspring, unless there are strong ecological and/or genetical advantages associated with cross fertilization (Maynard Smith 1978). If there are no such advantages to sex, a clone beginning with a single individual will replace a sexual population of 105 individuals in [less than]50 generations, and replacement of [10.sup.6] sexual individuals would occur in [less than]60 generations (assuming a 1:1 sex ratio [Lively 1996]). It is for this reason that explaining the maintenance of sexual reproduction in natural populations is a challenge for evolutionary theory (Williams 1975), and a large number of hypotheses for the advantage of sex have been presented in recent years (review in Kondrashov 1993). However, there is one condition that could convert the "challenge" for theory into a red herring. The challenge itself rests on an "all-else-equal" assumption, which asserts that offspring production by sexual and clonal females is similar (Maynard Smith 1978). If offspring production of clonal females is less than half that of sexual females, then the clone will diminish in frequency when rare, and the maintenance of sex is not problematical. In other words, without a true "cost of males" (Maynard Smith 1978), the hypotheses for the maintenance of cross fertilization remain as mental exercises (see Lamb and Willey 1979, Lynch 1984, and Bierzychudek 1987). The main criticism of the cost-of-males idea is that sexual and asexual lineages, although of common origin, may inherently show different fecundities (and life histories, in general) due to factors directly related to asexuality. For example, developmental difficulties associated with parthenogenetic egg production could be sufficient to prevent the spread of clones (Templeton 1982, Uyenoyama 1984), unless there is some way to selectively abort and replace defective embryos (Lively and Johnson 1994). Difference in ploidy is another factor that may cause differences in the life histories of the clonal and sexual individuals. Clones often have polyploid versions of diploid sexual genomes (Suomalainen 1962, Lynch 1984, Bierzychudek 1987); it is, therefore, not surprising that ploidy has been viewed as one possible explanation for commonness of sexual reproduction, and for its maintenance in natural populations. For example, one hypothesis that could explain the well-known association between high latitude and asexuality (Bell 1982, Bierzychudek 1987) is that there has been selection for a higher level of ploidy, not on the mode of reproduction per se (Vandel 1940, Suomalainen 1962). According to this hypothesis, clones are out-competed by sexuals in the common "sexual" environment; but due to enhanced trait expression associated with polyploidy, clones gain a competitive edge in some specific environments that are common in high latitudes. Some suggested examples of these specific conditions include low-diversity environments (Glesener and Tilman 1978), spatially homogeneous habitats (Bell 1982), and recently colonized habitats (Cuellar 1994).
The crux of discussions around ploidy, asexuality, and the maintenance of sex is that there may not be a paradox at all. This controversy is not easy to resolve, partially because of the different ways clones can be derived from sexual lineages. Polyploid asexual clones may be generated either through hybridization of sexual lineages (Vrijenhoek 1978b, Bierzychudek 1987, Radtkey et al. 1995), or directly from diploid sexual females (Innes and Hebert 1988, Havel and Hebert 1989, Chaplin et al. 1994, Little and Hebert 1994, Dybdahl and Lively 1995a, Theisen et al. 1995). These two main types of origin have significantly different implications for comparisons of clones to their sexual relatives. Hybridization combines two different genomes generating both novel allele combinations and elevated heterozygosity, while a direct switch to parthenogenesis freezes existing variation and preserves the existing genome (Vrijenhoek 1990). It may be expected that clones of hybrid origin are more likely to express phenotypes not found in the sexual relatives than clones resulting from a direct switch to parthenogenesis (see also Dybdahl and Lively 1995a).
In the present study, we subjected the all-else-equal hypothesis to test using sexual and asexual lineages of the freshwater snail Potamopyrgus antipodarum. Using field-collected data, we compared the life-history traits of non-hybrid triploid clonal females with their diploid sexual counterparts. To gain some ecological perspective, we contrasted the variation in life-history traits between sexual and clonal forms to the variation in life histories among habitats and sampling locations at our study site. We also conducted a laboratory competition experiment, where sexual snails competed with a single clone for 1 yr. Our results suggest that the maintenance of sex is a genuine paradox in these snails.
MATERIAL AND METHODS
Potamopyrgus antipodarum is a common proso-branch snail in the freshwater habitats of New Zealand (Winterbourn 1970). Sexual populations of the snail are dioecious, and females brood their offspring to the "crawl-away" stage of development in a brood pouch. Mixed populations of sexual and asexual individuals are common in New Zealand (Lively 1987). Parthenogenetic triploid females are frequently spun off from the diploid sexual populations (Dybdahl and Lively 1995a). Triploidy was confirmed with electrophoresis; however, the details of origin of asexuals are unknown (Dybdahl and Lively 1995a). One plausible explanation is production of diploid eggs that become fertilized with haploid sperm, producing a viable triploid in which balanced meiosis is blocked. Under this scenario, diploid parthenogens are expected to be rare (Saura et al. 1993). Our previous studies confirmed that diploid populations conformed to random mating and Hardy-Weinberg expectations (Dybdahl and Lively 1995a; Fox et al. 1996).
Lake Alexandrina (South Island, New Zealand) was selected as our study site because the snail population there is composed of diploid sexual individuals and triploid asexual individuals. Clonal diversity in the lake is exceptionally high (165 clones in 605 individuals) and structured with respect to habitat and site (Fox et al. 1996). From earlier studies, we also know that the distribution of parasite infections is spatially variable (Jokela and Lively 1995b), and that frequency of parasites is correlated with reproductive mode and size at maturity (Jokela and Lively 1995a).
Field collection, electrophoresis, and statistical analysis
In January and February of 1994, we collected snails from each of three littoral habitats at five different sites in Lake Alexandrina. The habitats were: (1) the shore-bank zone, consisting of willow roots and moss, (2) the Isoetes kirkii macrophyte zone at 1.5-3 m depth, and (3) the Elodea canadensis macrophyte zone at 46 m depth. Several hundred snails were collected at all 15 locations (3 habitats times 5 sites) by pushing a kicknet through the vegetation; the Isoetes and Elodea zones were collected by skin divers. For about 100 live snails from each of the 15 samples, shell length, gender, brood size, number of decaying embryos in the brood, and occurrence of trematode infections were recorded. The snails were then snap frozen with grinding buffer in liquid nitrogen for later cellulose acetate electrophoresis. Reproductive mode (ploidy) was inferred from asymmetric banding intensities of allozyme heterozygotes at two loci, from the frequency of allozyme genotypes (based on six polymorphic loci) compared to random expectations, and from the frequency of males within a multilocus genotype. (For details of electrophoresis and genetic analysis see Dybdahl and Lively 1995a, b, and Fox et al. 1996). Snails infected by digenetic trematodes are sterilized, and hence they were excluded from the data set prior to statistical analysis.
Key life-history traits for uninfected clonal and uninfected [TABULAR DATA FOR TABLE 1 OMITTED] sexual snails were compared using generalized linear models where applicable (McCullagh and Nelder 1983). Female size at maturity was analyzed with respect to mode of reproduction (ploidy), habitat, and transect using a three-way factorial ANOVA. [Growth of P. antipodarum stops at maturity (Winterbourn 1970), thus size of brooding individuals may be used as an estimate of size at maturity.] Total brood size (both live and dead embryos included) and effective brood size (live embryos only) were similarly analyzed using a three-way factorial ANCOVA, using shell length as a covariate. The effective brood size indicates the realized reproductive output after mortality of embryos has been taken into account, and total brood size indicates the theoretical potential for offspring production if all embryos survived during early development. The homogeneity-of-slopes assumption of ANCOVA was tested in both analyses by calculating the significance of covariate x factor interactions (all P [greater than] 0.05). The shore bank habitat had to be excluded from these analyses due to an insufficient number of clonal individuals. However, size at maturity and effective brood size of sexuals and clonal snails in the shore bank habitat were compared with Student's t tests, after the samples from all five transects were pooled. Asexual snails were present at all sites and clonal brooders (N = 8 individuals) were found on four of the five shore bank sites; therefore, pooling the shore bank samples does not create uncontrolled bias in the data.
To compare the variation due to mode of reproduction to the variation due to ecological factors (habitat, transect), we calculated partial effect-size estimates [partial eta squared: see Table 1 for formula and Norusis (1990) for details] for all effects in each ANOVA and ANCOVA. This estimate describes the amount of variation explained by each factor, thus allowing the estimation of the relative importance of mode of reproduction in explaining the observed variation in the measured traits. The analysis is analogous to partitioning the total variance into its components as in Model II ANOVA (Sokal and Rohlf 1981). To estimate the power of the t tests, we calculated the smallest detectable difference at P [less than] 0.05, using the sample sizes and standard deviations observed in the data.
The frequency of broods with decaying embryos (at least one decaying embryo in the brood), and proportion of brooders by mode of reproduction, habitat, and transect were analyzed with hierarchical logit models (see Salonen and Penttinen 1988 for an example). In this analysis the effects of each factor (ploidy, habitat, transect) were obtained by comparing models with and without that particular factor [partial chi-square analysis (Norusis 1990)].
The growth rates of sexual and clonal populations were compared in a competition experiment. Outbred sexual individuals (N = 120 snails) and individuals from a single clone (N = 65 snails) were placed together in 14 replicate 35-L tanks. Thus, at the start of the experiment 35% of individuals in each tank were clonal (65 out of 185). As controls, 185 sexual individuals were added to 4 additional tanks. The experiment was started in June of 1994. The clone (no. 51 in Fox et al. 1996) is the second most common clone found in the Isoetes habitat and in the shore bank habitat in Lake Alexandrina. Sexual and clonal snails used in the experiment originated from parents collected from Lake Alexandrina, and were kept in the laboratory for several generations before the experiment was started. Eleven months after the introduction of the snails (2-3 snail generations), we counted the snails in all 18 tanks. We also randomly selected 250 individuals from each tank and calculated the frequency of the clone. Clone 51 could be unambiguously distinguished from sexual individuals by the presence of a ridge on the outer whorls of the shell.
The change in the frequency of the clone through time was analyzed using hierarchical logit models (dependent variable: proportion clonal in the tank; factors: time, replicate). The effects of single factors (time, replicate) were obtained by comparing models with and without that particular term (partial chi-square analysis [Norusis 1990]). The relative growth rate for the clonal and sexual population in each tank was calculated by dividing the number of individuals at the end of the experiment by the number at the start. The deviation of mean growth rate of sexual and clonal populations from one ([H.sub.0]: "no growth") was tested against the t distribution. The relative growth rates of sexual populations in control tanks were then compared to the growth rates of sexual populations in tanks with clonal snails using the Mann-Whitney U test. Finally, the growth rates of clonal and sexual snails in 14 replicate tanks were compared with a pairwise t test.
Size at maturity differed between the Isoetes and Elodea habitats, but this difference was not attributable to reproductive mode (Table 1). Asexuals were on average 1.13% smaller than sexuals [ILLUSTRATION FOR FIGURE 1A OMITTED], but this small difference was not statistically significant (Table 1). Total and effective brood size in these two habitats indicated a statistically significant interaction between habitat and transect, but there was no significant effect of reproductive mode (Table 1). Sexuals had on average 2.99% larger broods than asexuals [ILLUSTRATION FOR FIGURE 1B OMITTED], but, as with size at maturity, this difference was small and statistically not significant (Table 1). Analysis within the shallow, shore-bank habitat yielded a similar result; size at maturity of sexual and clonal snails was almost identical, and although sexuals had slightly larger broods, the difference was not statistically significant (Table 2). Furthermore, reproductive mode explained a small, nonsignificant portion of the variation in size at maturity and total/effective brood sizes when compared to ecological factors (Table 1). Analyses of the frequency of broods with decaying embryos and the proportion of brooders in the samples suggests that reproductive mode had little to do with variation in these traits ([ILLUSTRATION FOR FIGURE 1C-E OMITTED], Table 3). Taken together, the results suggest that key elements of reproductive schedule were similar for triploid clonal and diploid sexual snails in the field, and that the number of developmental errors among offspring was not related to mode of reproduction.
Field data indicated that the life history traits of clone 51, which was used in the laboratory experiment (Results: Laboratory experiment), did not differ markedly from the sexual population. We detected no difference between the clone and sexual snails in size at maturity (t = 1.12, df = 75, P = 0.268), total or effective brood size (t = 1.43, df = 75, P = 0.157, and t = 1.64, df = 75, P = 0.105, respectively), or frequency of broods with decaying embryos ([[Chi].sup.2] = 3.31, df = 1, P = 0.068). These tests were conducted by comparing brooding females of clone 51 collected from the Isoetes habitat to brooding sexual females in the same samples ([N.sub.sexual] = 61 individuals, [N.sub.clonal] = 16 individuals).
The results of the laboratory experiment showed a dramatic increase in clone 51 in all 14 tanks to which it had been added (from 35% to an average of 62% clonal, [ILLUSTRATION FOR FIGURE 2 OMITTED]). The change in clonal percentage during the experiment was statistically significant (effect = Time, [[Chi].sup.2] = 444.14, df = 1, P [less than] 0.001) as were the overall differences among the replicates (effect = Replicate, [[Chi].sup.2] = 40.08, df = 13, P [less than] 0.001). The differences among the replicates indicate that demography of the populations (survival, fecundity) during the experiment varied among the tanks. Furthermore, the interaction between percentage change and replicate was significant, indicating differences in the magnitude of growth of clonal population in replicate tanks (effect = Time x Replicate, [[Chi].sup.2] = 29.64, df = 13, P [less than] 0.001). Relative growth rate of sexual populations was not higher in controls than in the tanks with the clonal snails (Mann-Whitney U = 19.00, P = 0.399). Relative growth rate of sexual populations averaged 3.91 [+ or -] 0.467 (mean [+ or -] 1 SE, N = 18 replicate tanks) and of clonal population 11.30 [+ or -] 1.471 (N = 14 tanks), both significantly different from 1 (t = 6.43, P [less than] 0.001 and t = 7.00, P [less than] 0.001, respectively). However, the relative growth rate of the clonal population was significantly higher than that of the sexual populations (mean difference = 7.74, pairwise t = 7.14, df = 13, P [less than] 0.001). Thus there is direct experimental evidence for a cost of males in P. antipodarum.
That there is either a genetic or an ecological cost to sexual reproduction is a fundamental assumption in the current controversy regarding the maintenance of sex in natural populations. So it is surprising that there have been very few direct evaluations of the cost in the wild. In the present study, we found that triploid, clonal Potamopyrgus antipodarum did not differ in key life-history traits from diploid, sexual individuals. In addition, the results of our laboratory experiment were consistent with the idea that clones can spread in sexual populations in the absence of selection for cross-fertilized offspring. These results are consistent with Maynard Smith's (1978) idea of a cost of males, and suggest that the maintenance of sex in these snails in nature requires strong selection either for variable offspring or for the mutation-clearing effects of meiosis and recombination.
In the only other field study known to us where life histories of mixed populations of sexuals and asexuals were extensively studied, Michaels and Bazzaz (1986) reported a higher seed production, but smaller seeds and lower survival, of apomictic Antennaria parlinii when compared to sexual conspecifics. Apomictic and sexual A. parlinii are both hexaploids, thus this difference is likely to be due to mode of reproduction. Michaels and Bazzaz suggested that the result may be due to clonal selection for traits beneficial for colonization, but unfortunately they had no data on clonal diversity. Several other studies have compared sexual and asexual species/lineages either in the laboratory or in the field (Uzzell 1964, Congdon et al. 1978, Schenck and Vrijenhoek 1986, Mitter and Klun 1987, Browne et al. 1988, Mladenov and Emson 1990, Mackay et al. [TABULAR DATA FOR TABLE 2 OMITTED] 1993, Zeyl et al. 1994, Radtkey et al. 1995, Snell and Carmona 1995). However, only a few life-history traits tend to be reported in these studies. Lynch (1984) reviews the literature published before 1984, and concludes that although some studies show the two-fold cost of sex, in most studies the performance of parthenogenetic lineages is poorer than that of sexuals. However, most of the studies reviewed in Lynch (1984) have been done with parthenogens of interspecific hybrid origin, or by comparing non-hybrid parthenogen species to the "closest" available sexual relative (not necessarily the one that the parthenogen was derived from). Thus, direct comparisons of sexuals and asexuals in the same habitats are rare (but see Michaels and Bazzaz 1986).
In this study, the life-history characteristics of the local clonal population, especially size at maturity, matched very closely the characteristics of the local sexual population, even within habitats [ILLUSTRATION FOR FIGURE 1 OMITTED]. Size at maturity, brood size, and proportion of brooders in the samples showed spatial variation, either among habitats, or as an interaction between habitat and transect. In all these traits, both diploid sexuals and triploid [TABULAR DATA FOR TABLE 3 OMITTED] clones expressed similar variation across habitats and transects, as indicated by the lack of statistically significant interaction terms with mode of reproduction. Together with the results of earlier genetic studies, according to which the clones are spun off locally from the sexual population (Dybdahl and Lively 1995a), and the observation that the genetic structure of clonal populations is organized by habitat (Fox et al. 1996), the results of the present study suggest that clones "freeze" the phenotype (including life-history traits) of the sexual genome from which they originate (see Vrijenhoek 1984).
Parthenogenetic individuals are generally thought to suffer from a higher frequency of developmental problems, such as poor hatching success of eggs (Lamb and Willey 1979, Lynch 1984), or lower egg production (Enghoff 1976, Taylor 1981). In animals, the same problems have been reported to be associated with polyploidy (Suomalainen 1962). Our results suggest that in P. antipodarum polyploidy was not associated with any consistent changes in the phenotype of the snails, and developmental problems did not seem to plague clonal offspring in any greater frequency than sexual offspring [ILLUSTRATION FOR FIGURE 1 OMITTED]. There are at least two possible reasons for these seemingly contradictory results. First, the high clonal diversity in P. antipodarum (Dybdahl and Lively 1995a, Fox et al. 1996) may include clones that are of recent origin, which do not carry the harmful mutations commonly thought to be partly responsible for developmental problems. Second, it may be that triploidy, when not a result of an interspecific hybridization, does not assemble the harmful allele combinations that might interfere with offspring development.
The origin of P. antipodarum clones probably results from fertilization of a diploid egg by a haploid sperm (or vice versa). It does not include interspecific hybridization. This is indicated by lack of novel alleles in clones, and by similar heterozygosities of the clones and sexuals (Dybdahl and Lively 1995a). However, in hybrid clones, polyploidy is often associated with differences in morphology, stress tolerance, fecundity, or other characteristics (Suomalainen 1962, Lynch 1984, Bierzychudek 1987). Furthermore, clones of hybrid asexual vertebrates have been reported to have different microhabitat preference and diet selection than sexuals (Vrijenhoek 1978a, b, 1984, Schenck and Vrijenhoek 1986, Bolger and Case 1994). Therefore, we suggest that the alterations in phenotypic characteristics, ecology, and behavior are more likely in clones of hybrid origin than in non-hybrid parthenogens. If true, this would suggest that maintenance of sex hypotheses - to which the cost of males is essential - are more relevant for non-hybrids than for interspecific hybrids. More studies of life-history traits of clones and their parental sexual lineages are needed to test this idea.
Our laboratory competition experiment showed a significantly faster growth rate of the clone compared to the coexisting sexual population. In addition, the final population sizes in the tanks varied several fold, indicating differences in the demography (fecundity/survival) of the populations among tanks [ILLUSTRATION FOR FIGURE 3 OMITTED]. This large variation among replicates indicates that the tanks provided different environments for the snails. While we cannot determine the cause of this variation, we welcome it; replicating the experiment in different environments makes for a more robust test. The cost of males, as measured by relative growth rates, varied among tanks (as indicated by the significant interaction between replicate and reproductive mode); but the growth rate of the clone was clearly faster than the sexual population in all 14 tanks [ILLUSTRATION FOR FIGURE 3 OMITTED]. Thus, the cost of males seems to hold across different conditions. Nonetheless, it is difficult to know whether the range of variation in the lab encompassed field conditions (see Moore 1975, 1976). Hence, our laboratory experiment showed only that it may be possible for a clone to displace sex under certain conditions.
Taken together, our results suggest that there is a cost of males in P. antipodarum as suggested by theory, which raises the question of why sexual individuals have not been replaced by one or more clones in the wild. One idea that has gained recent attention is that parasites select against common genotypes, and thereby prevent clones from becoming so common as to replace the sexual ancestor (the Red Queen hypothesis) (Jaenike 1978, Hamilton 1980, Hamilton et al. 1990, Howard and Lively 1994). It is not known at present whether time-lagged selection of this kind maintains sex in populations of P. antipodarum, but such selection is consistent with the biogeographic distribution of sex in these (Lively 1987, 1992, Jokela and Lively 1995a) and other freshwater snails (Schrag et al. 1994).
We thank E. Levri for help in the field, K. Obye and D. Zynger for help with the laboratory experiment, L. Delph, P. Mutikainen, T. Stadler, S. Weeks, T. Case, and one anonymous reviewer for comments on the manuscript, and the faculty and staff in the Zoology Department at the University of Canterbury for their continued support, especially M. Winterbourn, I. McLean, J. McKenzie, and J. Van Berkel. This study was supported by grants from the Academy of Finland (to J. Jokela), the U.S. National Science Foundation, and the Marsden Fund of New Zealand (contract LL 0501) (to C. M. Lively).
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|Author:||Jokela, Jukka; Lively, Curtis M.; Dybdahl, Mark F.; Fox, Jennifer A.|
|Date:||Mar 1, 1997|
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