SEARCH

SEARCH BY CITATION

Keywords:

  • asexual reproduction;
  • Centrocestus;
  • Melanoides tuberculata;
  • Red Queen hypothesis;
  • sexual reproduction

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

The Red Queen hypothesis predicts that sex should be more common in populations heavily infested with parasites, than in those without. This hypothesis was investigated in the aquatic snail Melanoides tuberculata, in which both sexual and parthenogenetic individuals exist in natural populations, and some populations are heavily infested by trematodes. The presence of fertile males and the higher genetic diversity of bisexual populations are indicative of sexual reproduction. We compared sites in 1990, 1999, and 2001, and we looked for a positive correlation between male and parasite frequencies. Male frequency was not correlated with the frequency of individuals infected by trematodes. This lack of correlation was reconfirmed in a retrospective power analysis. In a period of 9 years, male frequencies decreased but infection levels increased. These results do not support the Red Queen hypothesis. In samples with high male frequency the number of embryos was low, perhaps indicating that males may have a negative effect on embryo numbers. This effect of males on fitness could perhaps suggest that the cost of sex is fewer embryos. The reduction in embryo numbers may also represent a trade-off between mating and egg production costs.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

In nature sexual reproduction is the most abundant reproductive strategy among multicellular eukaryotes and many theories attempt to explain its abundance. The Red Queen hypothesis argues that sexual reproduction will be favoured when virulent parasites exert a time-lagged, negative frequency-dependent selection on their hosts (Van Valen, 1973; Jaenike, 1978; Bremermann, 1980; Hamilton, 1980; Bell, 1982; Hamilton et al., 1990). More precisely, the ‘two-fold cost’ disadvantage of sex (Maynard-Smith, 1971, 1978; Williams, 1975) can be overcome by the inability of clonal populations to cope with the rapid adaptation of parasites to common host genotypes. An alternative hypothesis, Müller's ratchet, argues that the accumulation of deleterious mutations in clonal genomes can explain the success of sex. This hypothesis is based upon population size in stochastic models (Müller, 1964), or mutation rate in deterministic models (Kondrashov, 1982, 1988), and does not rely on environmental factors. A recent pluralist approach suggests that the simultaneous interaction between the ecological (Red Queen) and mutational (ratchet) hypotheses may provide the necessary explanation for the advantage of sex (Howard & Lively, 1994, 1998; Lively & Howard, 1994; West et al., 1999).

Much of the empirical evidence supporting the Red Queen hypothesis comes from studies on the freshwater snail Potamopyrgus antipodarum (Gray, 1843) that can reproduce both sexually and without a mate. In this snail, a positive relationship between male frequency and infection level was found regardless of habitat (Lively, 1987, 1992; Jokela & Lively, 1995a; Lively & Jokela, 2002); the parasites were also more infective to snails from their local host populations (Lively, 1989; Lively & Jokela, 1996), suggesting a local adaptation that results from parasite tracking of locally common host genotypes (Lively & Dybdahl, 2000). The frequency of sexual individuals was high in shallow waters, where infection by parasites was highest (Jokela & Lively, 1995b). Clonal diversity was high in deep water (Fox et al., 1996), where clonal and sexual populations did not differ in the prevalence of infection (Jokela et al., 1997b). Life-history traits such as female size at maturity, brood size, and frequency of developmental errors in brooded embryos were not attributable to any reproductive mode, and thus suggested that a cost of sex does indeed exist (Jokela et al., 1997a). Dybdahl & Lively (1996) found that parasite dispersal rates were higher than those of their hosts, despite the correlation between population structures of parasites and hosts, and their relation to the spatial arrangement of the habitats. Dybdahl & Lively (1998) also demonstrated host cycling resulting from a time-lagged correlated response by parasites.

Another freshwater snail that reproduces both sexually and asexually is Melanoides tuberculata (Müller, 1774) (Family Thiaridae). Most populations reproduce through obligate apomixis (Jacob, 1957, 1958; Berry & Kadri, 1974), but male frequencies reach up to 40% in the French West Indies (Samadi et al., 1998), and up to 66% in Israel (Livshits & Fishelson, 1983; Heller & Farstey, 1990). Where males are present they have ripe gonads and motile sperm (Hodgson & Heller, 1990), and allozyme electrophoretic studies suggest cross-fertilization within the population (Livshits & Fishelson, 1983). Livshits et al. (1984) found that within the same geographic region, parthenogenetic populations were less diverse than bisexual populations. Heller & Farstey (1990) argued that a higher frequency of fertile males combined with the higher genetic diversity of bisexual populations is indicative of sexual reproduction. Microsatellite characterization did not reveal genetic differences between males and females in populations from the French West Indies (Samadi et al., 1998), but substantial genetic variation, found in populations from Morocco and Oman, may point to the existence of sexual (diploid) forms coexisting with asexual (polyploid) forms (Samadi et al., 1999).

Melanoides tuberculata serves as the first intermediate host to several species of digenetic trematodes, of which Centrocestus sp. is most abundant in Israel. The parasite sterilizes the snail, and cercariae liberated from snails encyst on the gills of fish, prior to being transmitted to waterfowl or waders (Farstey, 1986).

Given the high number of embryos in the brood chamber of the snail (Berry & Kadri, 1974; Livshits & Fishelson, 1983), and the sterilizing effect of the parasite, infection may alter the growth rate of a host population (May & Anderson, 1983). Melanoides tuberculata may also exhibit gigantism in response to parasite infestation (Minchella, 1985).

In Israel, Heller & Farstey (1990) (Fig. 1) surveyed Melanoides sites and recorded male frequency, trematode infection, faunal diversity, and water chemistry. They found that male frequency of M. tuberculata was not related to trematode infection: neither to their overall frequency, nor to the frequency of those parasites that could be identified specifically. Their results do not support the view that sex is favoured by selection resulting from host-parasite interactions.

image

Figure 1. Frequency (black) of parasite and male Melanoides tuberculata at various sites in Israel in 1990 and 1999. The 1990 male frequencies are redrawn from Heller and Farstey. The parasite frequency is gleaned from their Table 1. Male frequency: (a) 1990, (c) 1999; Parasite frequency: (b) 1990, (d) 1999.

Download figure to PowerPoint

Detailed experimental and genetic studies may assess whether parasites track common clonal host genotypes, but the first step in any such research is to establish whether male-vs.-infection correlations occur repeatedly, in natural populations.

The purpose of this study was to examine, in M. tuberculata, if the prediction of the Red Queen hypothesis, that parthenogenesis is favoured in the absence of parasites, is realized. We tested this prediction by investigating male and infection frequencies over time, by comparing sites sampled by Heller & Farstey (1990) after 9 and 11 years, and in space, by seeking a positive correlation between male and parasite frequencies, in 59 sites in Israel. We also looked for alternative factors affecting these frequencies, such as habitat geography and habitat type.

Furthermore, assuming that embryo numbers represent some broad indication of reproduction ability, we examined the effects of males and parasites on fitness. We did so by seeking a correlation between male and infection frequency on the one hand, and embryo numbers on the other. We looked for any additional fitness costs imposed on sexuals, besides the two-fold cost of meiosis.

Materials and methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

A survey of 59 previously known freshwater sites was carried out in Israel during the summer of 1999 (first survey). During the summer of 2001 nine sites common to both the Heller & Farstey (1990) survey and our first survey were sampled again (second survey). In both surveys a random sample of 100 snails was collected from each site. A sample of this size can discriminate between sexual and asexual populations; for example, given a sexual population with at least 10% of males, the probability of finding less than 2% of males in a sample of 100 snails, and thus erroneously concluding that the population is asexual, is <3.84 · 10−3 (99% CI 0–9.73% when n = 100).

Adult snails were transported alive to the laboratory, where they were sexed by holding an intact snail up to a strong light (see Heller & Farstey, 1989). On a couple of occasions we found very few dead snails, which could not be analysed and were thus removed from the sample. Next, shell-height of each snail was measured to an accuracy of 0.01 mm, and then the number of embryos in the brood pouch of females was counted. Finally, trematode infection was determined by examining the gonad and digestive gland under a light microscope. Sites were grouped into three categories by habitat geography (valley, coast or desert) and into four categories by habitat type (stream, lake, pond or spring). These categorical predictor variables were ‘dummy’ recoded into uncorrelated dichotomous variables (contrasts), before entering them into a regression model.

For statistical analysis, SPSS for Windows v. 10.0.5 (SPSS Inc., 1999) was used. Mean values are shown with ±SD. Frequency data were arcsine (square root) transformed before being analysed. All probabilities are two-tailed. Parametric tests were used whenever possible, based upon Kolmogorov–Smirnov's test of normality with Lilliefors significance correction (for large samples, n > 50), or Shapiro–Wilks’W-test (n ≤ 50). The equality of variances assumption for anova was verified using Levene's test of homogeneity of variances. Contingency tables were tested using the likelihood ratio test. Power analysis was performed using G*POWER (Erdfelder et al., 1996).

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

Fifty-nine sites, originally aquatic according to Heller & Farstey (1990) and geographical maps, were examined on the first survey. Of these only 27 were found to be still aquatic and of those only 23 were inhabited by M. tuberculata (Fig. 1). Of the 34 sites surveyed by Heller and Farstey in 1990 only nine contained M. tuberculata; another seventeen were dry, and eight contained water but no M. tuberculata. From these results it might perhaps be argued that M. tuberculata inhabits temporary habitats and that it is prone to high extinction rates. However, most of the now-dry habitats were destroyed by man. Thus in northern Israel, En Avazim and En Kaftor have become resting places for cattle, and Nahal Oren and En Husha have been diverted for irrigation. In southern Israel drought, overuse of water or a combination of the two has left many places dry. Once-rich springs bordering Ein Fashkha are now dry because of human-induced drop in sea level of the Dead Sea, which causes a continuous drop in the once higher aquifer and leaves many springs dry. Nevertheless, all the sites that we sampled in either year were undisturbed before and during sampling.

In the first survey (1999), the frequency of M. tuberculata males varied between 0 and 37.5% (Fig. 1). Ten of the 23 sites contained no males, 10 contained <10%, and three had more than 10% males. The frequency of infected snails varied between 0 and 87.5% (Fig. 1). Six of the 23 sites contained no infected snails, and six were highly infected, with more than 35% infected snails.

In the second survey (2001), male frequency varied between 0 and 31.5% (Fig. 2). Two of the seven sites contained no males, four contained <10%, and one had more than 10% males. Infection frequency varied between 0 and 100% (Fig. 2). One of the seven sites contained no infected snails, and three were highly infected, with over 35% infected snails.

image

Figure 2. Frequency (black) of parasite and male Melanoides tuberculata at various sites in Israel in 2001. (a) Male frequency, (b) Parasite frequency.

Download figure to PowerPoint

In six of the seven sites surveyed by Heller & Farstey (1990) we found lower male frequencies and higher infection frequencies, in both our surveys. The distribution of infection prevalence was highly variable and skewed, and included populations with both low and high infection levels (Fig. 3).

image

Figure 3. Distribution of prevalence of infection.

Download figure to PowerPoint

We found no correlation between male frequency and infection level in either surveys (Table 1; Fig. 4). Both male and infection frequencies were not correlated with the mean number of embryos, or the proportion of females with embryos (Table 1). In the first survey, the mean number of embryos was 2.12 ± 5.23 for infected snails (n = 181) and 7.38 ± 12.57 for uninfected snails (n = 683); this difference is significant (Mann–Whitney U = 27 204.5; P < 0.001). A similar significant difference was obtained in the second survey (Mann–Whitney U =794.0; n = 70 and 158; P < 0.001).

Table 1.  Correlation coefficients, for our two surveys and for the data of Heller & Farstey (1990)*.
Variables comparedHeller & Farstey, 1990 (n = 34) Pearson r (P, 2-tailed) First Survey 1999 (n = 23) Pearson r (P, 2-tailed)Second Survey 2001 (n = 7) Spearman rho† (P, 2-tailed)
  1. *Data re-analysed by applying the arcsine (square-root) transformation.

  2. †A nonparametric test because of the small sample size.

  3. ‡Mean embryos were log-transformed.

Male frequency and infection−0.022 (n.s.)−0.353 (0.099)−0.270 (n.s.)
Male frequency and mean embryos‡n/a−0.336 (n.s.)−0.252 (n.s.)
Male frequency and females w/embryosn/a−0.124 (n.s.)−0.748 (0.053)
Infection and mean embryos‡n/a0.085 (n.s.)−0.607 (n.s.)
Infection and females w/embryosn/a0.097 (n.s.)0.037 (n.s.)
image

Figure 4. Male frequency vs. infection frequency in Melanoides tuberculata in Israel (1999, 2001).

Download figure to PowerPoint

In the first survey, the mean number of embryos decreased as male frequency increased (no males: 9.59 ± 16.09, n = 340; <10% males: 6.19 ± 7.52, n =306; over 10% males: 3.14 ± 4.84, n = 86; Kruskal–Wallis χ2 = 28.83, P < 0.001). This pattern repeated itself in the second survey (no males: 13.97 ± 8.09, n = 37; <10% males: 9.54 ± 6.90, n = 107; over 10% males: 7.21 ± 4.33, n = 24; Kruskal–Wallis χ2 = 15.19, P < 0.001).

Mean shell height of infected and uninfected snails differed significantly in the first survey (infected: 18.98 ± 4.60, n = 181; uninfected: 16.03 ± 3.87, n =721; Mann–Whitney U = 39955.5, P < 0.001), and in the second survey (infected: 18.42 ± 3.75, n = 71; uninfected: 14.71 ± 2.34, n = 173; Mann–Whitney U = 2573.0, P < 0.001). However, the partial correlation between male frequency and infection level in the first survey, when controlling for the effect of mean shell height (or age), was still nonsignificant (partial r = −0.303; n = 23; P = n.s.). A low but significant correlation was found between shell height and the number of embryos in the first survey (Pearson r =0.287; n = 732; P < 0.001), and in the second survey (Pearson r = 0.199; n = 168; P < 0.01).

When comparing data from Heller & Farstey (1990) and our two surveys (from 1999 and 2001), male frequencies differed significantly (1990: 30.2%, 1999: 4.9%, 2001: 8.7%; Likelihood ratio G = 240.78; d.f. = 2; P < 0.001). Infection frequencies, however, significantly increased over the years (1990: 5.9%, 1999: 20.1%, 2001: 29.1%; Likelihood ratio G = 149.76; d.f. = 2; P < 0.001). When only comparing our two surveys male frequency did not differ significantly (Likelihood ratio G = 3.54; d.f. = 1; P = 0.06), but infection level, once again, increased significantly (Likelihood ratio G = 8.70; d.f. = 1; P < 0.01).

Habitat geography was significantly correlated with male frequency in the first survey (Table 2). Forcing infection level as the first variable entered in a stepwise multiple regression analysis, confirmed our previous finding that male and infection frequencies were not correlated. The second survey was not analysed because of the small sample size. Between-habitat type categories, male frequency and infection level differed significantly in both surveys (Table 3; Fig. 5). A similar significant difference between habitat geography categories was obtained in both surveys for male frequency, but only in the second survey for infection level.

Table 2.  Stepwise multiple regression analysis† for the first survey.
Step/sourceRegression MS (d.f.)Residual MS (d.f.)FTotal R2
  1. *P < 0.01; infection level was a nonsignificant source (P = 0.099), as well as all other contrasts.

  2. †The dependent variable was male frequency; independent variables were infection level, habitat geography and type (after being recoded into contrasts). MS, mean square.

No variables forced
 1 Desert vs. coast/valley0.268 (1)0.018 (21)15.03*0.417
Infection level forced
 1 Infection level0.080 (1)0.027 (21)2.990.125
 2 Desert vs. coast/valley0.149 (2)0.017 (20)8.63*0.463
Table 3.  Male frequency and infection level within habitat geography and habitat type†.
SourceHabitat geography G (d.f.)Habitat type G (d.f.)
  1. *P < 0.001.

  2. †We used the likelihood ratio test to examine the differences in male frequency and infection level within habitats.

Male frequency, first survey, 199957.23* (2)46.74* (3)
Male frequency, second survey, 200143.46* (2)43.74* (2)
Infection level, first survey, 1999 5.42 (2)32.58* (3)
Infection level, second survey, 200117.52* (2)27.51* (2)
image

Figure 5. Male frequency and infection level within habitat type and geography in the first (1999) and second (2001) surveys. Habitat type: (a) 1999, (b) 2001; Habitat geography: (c) 1999, (d) 2001.

Download figure to PowerPoint

An essential requirement for confirming the lack of correlation between sexuality and parasitism is a formal power analysis. Such an analysis is necessary to clarify the issue of whether no detection means actual absence or inadequate power. As our first survey initially consisted of 59 potential sites, we performed prospective (a priori) power analysis (Cohen, 1988) and obtained effect size r = 0.32 for a one-tailed test at α = 0.05 and β = 0.8. Higher effect sizes (r = 0.39–0.58) were observed in comparable surveys (Lively, 1987, 1992; Lively & Jokela, 2002). However, only 23 sites were actually inhabited by M. tuberculata and within those sites male-infection correlation was found to be nonsignificant. Thus the prospective power of our study, based upon effect sizes from comparable surveys, ranges between β = 0.62–0.95. In other words, the detectable effect size for a one-tailed test at n = 23, α = 0.05, and β = 0.8 is r = 0.48. We therefore performed retrospective (post hoc) power analysis and calculated a confidence interval (CI) around the observed effect size (Thomas, 1997). Given the negative correlation between male frequency and infection level, we obtained a 95% CI (−0.668, 0.069). Taken together these analyses provide assurance that sexuality and parasitism are indeed not positively correlated based upon a sample of only 23 sites.

The different types of habitats may obscure any correlation between sexuality and parasitism, especially in light of the low number of sites. However, except for the effect of desert (Table 2), which explains 42% of the variation in males, none of the remaining variables is significant. The partial correlation between sexuality and parasitism, when removing the effect of desert, is still negative and insignificant (partial r = −0.281; n = 23; P = n.s.). Even after forcing all five habitat contrasts into the model the partial correlation remains insignificant (partial r = −0.411; n = 23; P = 0.09). In addition, there is no evidence of collinearity between the predictors variance inflation factor (VIF) (ranges from 1 to 1.28). Finally, a 95% CI for these latter partial correlations supports our findings that sexuality and parasitism are still not positively correlated.

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

The Red Queen hypothesis predicts that parthenogens should be more parasitized than sexuals, and in P. antipodarum in New Zealand there is indeed evidence of this prediction. However in this study, of M. tuberculata in Israel, sexuality and parasitism were not correlated in either the 1990, 1999 or 2001 surveys. Our results do not offer evidence to suggest that male frequency is affected by parasites. In the period since the 1990 survey, male frequencies decreased whereas infection levels increased. We have no suggestion as to what abiotic or biotic factor may be responsible for these changes, in male and parasite frequencies, over the study period.

The environmental parameters we tested for influence on male and infection rates were habitat geography and habitat type. Concerning habitat geography, in the first survey there were more males in the desert than in the Jordan Valley and Mediterranean coast. This might perhaps seem to be explained by geographic parthenogenesis, and its claim that parthenogens tend to occupy disturbed habitats (Lynch, 1984), thereby suggesting that desert habitats are less disturbed. However, in re-analysing the 1990 data of Heller and Farstey, no differences were found in male frequency relating to habitat geography. This lack of consistency between surveys implies that male dispersal is random in geographic terms. Infection rates did not differ consistently between the geographic groups, suggesting that parasite prevalence was not influenced by habitat geography.

Between habitat types, in both surveys of this study male frequency was higher in springs and streams than in lakes and ponds, and infection level was higher in springs. In the re-analysed data of Heller & Farstey (1990) we did not find such differences.

We also examined the effect of males on fitness. These effects include the cost of mating or copulation (Fowler & Partridge, 1989), which together with the cost of egg production (Chapman et al., 1998) constitute the cost of reproduction. In samples with high male frequency the number of embryos was low, perhaps indicating that males may have a negative effect on embryo numbers. This could suggest that the cost of sex is fewer embryos, but we do not know if there is differential survivorship between sexual and asexual embryos. The reduction in embryo numbers may also represent a trade-off between mating and egg production costs, in which sexual females subject to increased mating costs produce fewer embryos.

In mollusks, support for the Red Queen hypothesis was found, besides Potamopyrgus, also in the freshwater gastropod Campeloma decisum (Say, 1817), where a higher level of parasitism in parthenogenetic populations than in sexual ones was found (Johnson, 1994). However, in some cases when the risk of infection was low, uniparental reproduction was associated with low levels of infection by parasites (Johnson et al., 1995). In Campeloma limum (Anthony, 1860), where both sexuals and parthenogens occur, parthenogens persist by higher dispersal rates into marginal habitats, thereby escaping from trematodes and minimizing competition with sexuals (Johnson, 2000). In organisms other than mollusks, support for the Red Queen hypothesis was found in a fish (Lively et al., 1990), a lizard (Moritz et al., 1991), a frog (Chandler et al., 1993), and a flatworm (Michiels et al., 2001). Situations that do not conform to the Red Queen hypothesis were found in geckos (Hanley et al., 1995), a fish (Weeks, 1996), a freshwater bryozoan (Vernon et al., 1996), and in Drosophila and its hymenopterous parasitoids (Kraaijeveld & Godfray, 1999).

The Red Queen hypothesis requires a virulent parasite, yet our results indicate that some infected snails were still carrying embryos. However, a closer examination reveals a different pattern: in the first survey 116 of 683 uninfected females (17.0%) were not carrying embryos, compared with 131 of 181 infected females (72.4%). This pattern repeated itself in the second survey: 9 of 158 uninfected females (5.7%) were not carrying embryos, compared with 59 of 70 infected females (84.3%). We therefore speculate that infected snails brooding offspring were in the initial stages of infection, prior to sterilization.

Stochastic processes may interfere with coevolutionary interactions, especially within small populations. These perturbations may in turn influence the dynamics of individual clones and sexual lineages (Howard, 1994), as well as host-parasite interactions. However, based upon our data and previous studies by Heller & Farstey (1990), and given the short time (5 min) we spent in collecting 100 snails per sample, we estimate snail population size in all sampling sites to be well above 10 000 individuals, thereby minimizing the risk of stochastic interference.

Lively (2001) recently suggested that sexual reproduction should be positively correlated with infection level only if the range of prevalence is wide, with very low and high prevalence. Yet our results show a highly skewed distribution of populations (Fig. 3), with no apparent correlation between sexuality and parasitism (Table 1; Fig. 4).

The apparent lack of correlation between male frequency and parasite prevalence may have other sources. Given that sexually-reproducing snails are relatively rare within many asexual populations, it could perhaps be argued that genetic variation within these small sexual subpopulations may be relatively low, so that any benefits that sex may provide would be much reduced. However, even in predominantly asexual populations of M. tuberculata, genetic studies revealed substantial genetic variation between sexual and asexual forms (Livshits et al., 1984; Samadi et al., 1999). Dispersal and gene flow may also alter the outcome of Red Queen interactions. The habitats sampled are highly diverse and isolated, making dispersal of snails very difficult. The low vagility of adult M. tuberculata and the lack of effective dispersal stages (larvae) limit gene flow between populations (Myers et al., 2000) to random dispersal by migratory birds. Furthermore, Livshits et al. (1984) found that the average genetic identity between populations was low and that within the same geographic region sexual populations were more diverse than asexual ones. We have therefore assumed that the populations sampled are indeed separate populations.

Studies of Red Queen dynamics using snails have traditionally been analysed on a one-on-one basis, involving a single host vs. one parasite species. Yet hosts are rarely infected by only one type of parasite and little is known about the interactions between the parasites and their effects on the host (Webster & Davies, 2001). Our study is no exception and infection by other parasite species may very well reveal a correlative increase in sexually reproducing populations, as predicted by the Red Queen hypothesis.

An alternative explanation stems from another major prediction of the Red Queen hypothesis, that infection should be genotype-specific, with time-lagged dynamics. If male frequency lags behind infection level (or the opposite), then there would be some points in time in which male frequency is not correlated with parasite prevalence. In either case, this prediction will be verified by examining genotype frequency within individual populations.

To conclude, much of the current research on mollusks supports the Red Queen hypothesis, but these studies were on only two genera. It is therefore important to test the hypothesis in different species and to test its ability to be a general hypothesis. This paper suggests that evolutionary consequences based upon male-parasite correlations found in Potamopyrgus cannot be detected in Melanoides.

Acknowledgments

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

D. Cohen and C. Lively kindly criticized an earlier version of this manuscript. We are grateful to U. Motro and Y. Ritov for statistical advice. Three anonymous reviewers provided suggestions and valuable comments that greatly improved the manuscript. Specimens for this study were collected under permit 6094 from the Israeli Authority for Nature Reserves and National Parks. This study was supported by a Horwitz Foundation Fellowship to F.B.A.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References