Behavioral Ecology Advance Access originally published online on June 30, 2004
Behavioral Ecology 2004 15(6):976-981; doi:10.1093/beheco/arh101
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Body size–dependent gender role in a simultaneous hermaphrodite freshwater snail, Physa acuta
Department of Systems Sciences (Biology), University of Tokyo, Komaba, Meguro-ku, Tokyo 153-8902, Japan
Address correspondence to M. Shimada. E-mail: mshimada{at}balmer.c.u-tokyo.ac.jp.
Received 23 April 2003; revised 4 February 2004; accepted 21 February 2004.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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We examined whether gender role in the simultaneous hermaphrodite freshwater snail, Physa acuta, is determined by relative body size in a manner predicted by the size-advantage model. We observed the body-size combinations of pairs in the laboratory by using field-collected populations. Smaller individuals tended to play the "male" role (sperm donor), and larger snails the "female" (sperm recipient). Next, we analyzed the mating behaviors involved in gender-role decision in snail pairs of three different body-size combinations, using "large" and "small" snails. Smaller snails were more likely to approach the partner as a male in different-size combination (large/small), whereas frequent initial approaches as a male and rejection behavior as a female were observed in the large/large combination. Third, we examined the body size preference when a snail can freely choose the partner from two other individuals of different body sizes (large/large/small or large/small/small). Small individuals had a significant tendency to act as the male and positively selected large snails as the female partner in both triple combinations. However, the large individual acted as both the male and the female with nearly equal frequency. In the size-differing pairings, copulations occurred after fewer male approaches and fewer rejections than in pairings involving two large snails, suggesting that body size difference is one of the behavioral solutions in gender conflict. Clear gender-role switching associated with body size was not seen. Smaller snails thus have a tendency to play the male role more frequently but adopt both gender roles when their body size is sufficiently large.
Key words: freshwater snails, gender role, Physa acuta, simultaneous hermaphrodites, size advantage model.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The size-advantage model (Charnov, 1979
, 1982; Ghiselin, 1969; Warner, 1975) was developed to explain the timing of physiological/developmental sex change in sequential hermaphrodites, including plants (Ruhren and Handel, 2000; Zimmerman, 1991) and fishes (Carruth, 2000; Munday, 2002; Schärer et al., 2001; St. Mary, 1994). This model focuses on the relationship between body size and fitness gain for males and females. The size advantage model predicts that sex change is observed when the reproductive success of one sex increases more with the body size than that of the opposite sex (Charnov, 1979, 1982; Ghiselin, 1969, 1974; Warner, 1975).
Many have suggested that the model is theoretically applicable in predicting gender-allocation strategies in simultaneous hermaphrodites (Angeloni et al., 2002; Charnov, 1979, 1982, 1996; DeWitt, 1996; Schärer et al., 2001; St. Mary, 1994). In simultaneous hermaphrodites, adults have mature male as well as mature female reproductive organs, and can adopt either the male or the female role in mating (the gender role). Because a close relationship between body size and the timing of sex change is observed in sequential hermaphrodites, the gender role decision depending on body size might also be seen in simultaneous hermaphrodites.
Several studies have reported that female-role individuals are typically larger than are their male-role partners (Angeloni and Bradbury, 1999; DeWitt, 1954, 1996; Otsuka et al., 1980; Staib and Ribi, 1995; Tomiyama, 1996; Yusa, 1996). In this case, the larger one takes the female role, the small one the male role. Why is the gender role related to body size? Less energy is required to produce sperm than to produce eggs. In simultaneous hermaphrodites, some species continue to grow after sexual maturation. If the potential reproductive value of one gender role increases much more with body size than the other (e.g., the amount of sperm transferred per copulation, or the amount of eggs produced per litter), smaller individuals would prefer to act more frequently as a male and large enough ones as a female, or vice versa, as the size-advantage model predicts. Thus, they may decide to choose the more favorable role that reflects higher reproductive success, depending on body size.
In some simultaneous hermaphrodites, individual gender role is clearly separated between mating partners, with one acting as the sperm donor (the male role) and the other acting as the sperm recipient (the female role). We can distinguish individual gender roles easily in this case. This pattern of mating behavior has been reported for freshwater snails such as Lymnaea stagnalis (Barraud, 1956; van Duivenboden and ter Maat, 1988), Physa heterostropha, and P. gyrina (DeWitt, 1991).
There are only a few reports on testing the size advantage model in simultaneous hermaphrodites (Angeloni et al., 2002; DeWitt, 1996; Schärer et al., 2001; St. Mary, 1994). DeWitt (1996) reported that the female role snail of P. gyrina and P. heterostropha was larger than was the male role in a copulating pair in nature as well as in the laboratory. When a larger snail (acting as the male) approached a smaller one in an encounter, the latter was likely to show rejection behaviors (e.g., shell swinging; DeWitt, 1991). Thus, DeWitt provided the first empirical indication that the size-dependent gender role can be explained by applying the size advantage model even in simultaneous hermaphrodites. However, DeWitt (1996) did not report actual body size distributions within the observed populations. The distribution of body sizes could be such that by chance there are frequent encounters between individuals with large differences in their body sizes. Therefore, the real size distribution data of the population are necessary for more precise analysis. DeWitt (1996) also suggested that the preferred gender role for physid snails is to act as a male. Although the topic of preferred gender role is one of the central research subjects, this suggestion has never been tested in mating behavior experiments that controlled for body size differences between paired snails.
In the present study, we conducted experiments on mating behavior in order to determine whether the size advantage model can explain the relation between the body size and gender role in a simultaneous hermaphroditic freshwater snail, Physa acuta, which continues to grow even after sexual maturation. A hypothesis was constructed based on the size advantage model: small snails should prefer to act as the male, and large snails as the female. This hypothesis was initially based on the sequential hermaphroditic sex-changing pattern. However, different patterns of gender role change will be possible in simultaneous hermaphrodites because of their more flexible response to local conditions. When considering the snails limited mobility, the temporal dynamics of gender role may also depend on the relative sizes of individuals encountered locally, the possibility of sperm competition, the relationships of body size and male or female reproductive abilities, and so on. To test this hypothesis in field-collected Physa, we designed experiments to explore (1) the relation between body size differences and gender role with populations of known overall body size distribution (experiment 1), (2) mating behaviors related to gender decisions between two snails of different body sizes (experiment 2), and (3) gender preference under free mating choice in a triple combination (experiment 3).
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METHODS |
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Study organism
Physa acuta is a simultaneous hermaphrodite freshwater pulmonate that originated in Europe and is now abundant in ditches, rivers, streams, and ponds in Japan. Physid snails are simultaneous hermaphrodites that usually cross-fertilize but are capable of occasional self-fertilization, for example, P. heterostropha (DeWitt, 1991
; Dillon and Wethington, 1995; Wethington and Dillon, 1993, 1997) and P. acuta ( Jarne et al., 2000). Although self-fertilization has been reported in some genetic analyses (Monsutti and Perrin, 1999), it is suggested that they are, in principle, out-crossers. In a preliminary study, individuals being kept alone (selfing) throughout their life produced only about one-twentieth of the number of eggs (mean = 50.8 ± 50.6 [SD], n = 30), compared with multiple mating wild snails (986.9 ± 541.1, n = 113). Thus, we regarded that selfing is unlikely to have a significant effect on the availability of eggs or sperm in mating with other individuals in the present experimental system. We used production of self-fertilized eggs as an indicator of reproductive maturity in order to select individuals for our experiments.
Sexual roles are clearly separated between a male role snail (sperm donor) and a female role snail (sperm recipient). We can distinguish the individual gender role easily. Sperm transfer is always unidirectional (not reciprocal). Male mating behavior involves (1) approach and climbing onto the shell of an intended female, (2) crawling to the female gonophore, (3) preputium eversion for intromission (copulation lasts 5–15 min), and (4) dismounting. This mating behavior pattern and rejection behavior (shell swinging, biting, etc.) by a snail that receives an approach is similar to that of P. grina reported by DeWitt (1991).
Experiment 1: relationship between body size and gender role
Our goal in experiment 1 was to determine if body size affects the gender role of snails and, specifically, if male- and female-role individuals in a mating pair show consistent size differences in freely mating experimental populations. Our null hypothesis was that there would be no size difference between the male and the female in a copulating pair. The null hypothesis would be rejected if a size difference between the partners were observed and if smaller snails acted as the male and larger as the female.
We collected P. acuta snails from a ditch and a pond in Kakegawa (34°48' N, 138°01' E; Kakegawa-DITCH and Kakegawa-POND) and a ditch in Shimizu (34°80' N, 138°29' E; Shimizu-DITCH) in June 2001, all located in the western part of Shizuoka prefecture, Japan. The snails were brought into the laboratory, and each population was maintained separately for about 1 day in artificial pond water (Elliott and Benjamin, 1989), being fed with Tetra-Min powder, a food designed for herbivorous tropical fish. For mating observation, we put each population in a separate container (width x length x height = 28 x 40 x 17 cm) filled with 10 l of artificial pond water, and kept three containers under a daily light/dark regime of 16 h light and 8 h dark. Density in the experimental aquaria (about 0.5 snails per 10 cm2 in Kakegawa-DITCH [n = 117] and Kakegawa-POND [n = 112], and 1.1 snails per 10 cm2 in Shimizu-DITCH [n = 254]) was similar to that observed in the field during the reproductive season when we collected the samples (about 1.0 snails per 10 cm2).
Mating behavior was observed for 4 h during the dark phase at 25°C. When we identified a pair that had copulated, we took them out from the container and measured the weight of each snail to the nearest 0.1 mg. Snails were placed back into the container after measuring. After the 4-h observation, we measured the weight of every snail in the aquarium.
Individual body size was represented by the body weight. The shell width and length highly correlated with the body weight (shell width: r =.97, n = 51, p <.0001; shell length: r =.97, n = 51, p <.0001).
Statistical analysis
We used the variance ratio test based on an F distribution for log-transformed data to examine homogeneity of the body size variances between populations. We applied a binomial test to examine the relation between the size difference and the gender role in each pair. We conducted a bootstrap analysis (Manly, 1997; Smith, 1998) to test the size asymmetries owing to systematic size mismatches between sperm donor and recipient. With M being the number of observed mating pairs for 4 h, the mean pairwise body weight differences in M pairs formed by random sampling within each population was used as the test statistic. This generated a probability distribution of size mismatches under a null hypothesis that there is no overall mean difference between donor and recipient sizes. The bootstrap test was conducted for each population until M random pairings of 9999 sets were achieved, then we placed the observed mean pairwise size-difference against the probability distribution. If our observed value fell within the top 500 rank among 10000 sets in a population (5%), we concluded that there was significant size asymmetry using a one-tailed test.
Experiment 2: effect of relative body size on gender decisions in pairs of snails
To investigate the effect of relative body size on gender decisions, we created pairs of snails in the following size combinations: large/large, small/small, and large/small. Our null hypothesis for this experiment was that the relative body size of mating partners does not affect gender role decisions. The null hypothesis would be rejected if small snails adopted the male role and the large/small pair copulated more readily than two other combinations (large/large and small/small).
To distinguish two individuals within a pair, we used body color (albino and wild type). No other artificial marking technique (e.g., painting numbers or spots on the shell, drilling a mark on the shell) was effective in preliminary trials because of either damage to the snail or durability in water. We had collected one albino snail in Kakegawa, Japan, in August 1999. We raised this albino in the laboratory, collected eggs, and raised wild type and albino juvenile offspring separately (for the latter, produced by selfing). After they matured, they produced eggs, and we collected and raised these offspring separately until maturation and then used them for the experiment.
The inheritance of albinism is generally very complex (e.g., complementary inheritance in P. heterostropha; Wethington and Dillon, 1993), and the simple one locus/two allele model could not be applied in our case. However, the albino morph can be used as an individual marker because of their equivalent fecundity to the wild type.
During the mating observations, every pair was maintained in a 50-ml plastic centrifugation tube filled with 40 ml artificial pond water. Behaviors were observed under controlled conditions (25°C, 16-h light/8-h dark) for 16 h in total (4-h observations during the dark period for 4 consecutive days).
We used three combinations of body sizes, designating the same-size combinations of either large or small size as large/large (LL, n = 20) and small/small (SS, n = 18), respectively, and the heterosize combination as large/small (LS, n = 17). The large snails were twice as large as the small ones (large = 0.0467 ± 0.001 g, n = 60; small = 0.0231 ± 0.002 g, n = 60). The albino and wild-type individuals were randomly mixed in the LS combination, and we did not separate the data. We recorded the following courtship behaviors: (1) initial approach as the male role, (2) rejection behavior of the female role, and (3) copulation.
Statistical analysis
We compared the number of premating courtship behaviors among LL, SS, and LS pairs by using the nonparametric Kruskal-Wallis test. The mating probability per initial approach was tested by using Fisher Exact test. Successful copulation rate was not statistically tested because this is a population-level value and has no replication. We also compared mean initial approaches by the male role snails using the nonparametric Wilcoxon's signed-rank test.
Experiment 3: effect of body size on pair formation and gender role among snail trios
To investigate the gender role preferences of small individuals, we created trios of two large snails and one small snail (LLS) or two small snails and one large snail (SSL) and observed which individuals were involved in mating pairs and the gender roles assumed by small versus large individuals. Our null hypothesis was that mating pairs would form at random with respect to body size. The null hypothesis would be rejected if the small snails were more likely to act as the male and rarely took on the female role.
Snails were collected from a pond in Kakegawa in May and June 2002. We measured their weight and maintained them separately in the laboratory. We used two trio combinations, designating the combination of two large snails and one small snail as large/large/small (LLS, n = 42), and two small snails and one large snail as small/small/large (SSL, n = 31). The large snails were more than twice as large as the small ones (large = 0.088 ± 0.05 g, n = 150; small = 0.030 ± 0.01 g, n = 146).
The mating observations were conducted during the dark period, with the snails in a 50-ml plastic centrifugation tube filled with 40 ml artificial pond water. When the first copulation was observed, we recorded the gender role of each individual in the copulated pair and ended the observation.
Statistical analysis
First, we tested the null hypothesis of the body-size combinations of a pair kept randomly in a trio irrespective of the gender role. Calculation of random probability, for example, in the LLS trio, is as follows. Possible copulation-pairings involving body size and gender role combinations can be (a) L-female and S-male, (b) S-female and L-male, and (c) L-female and L-male. If pairings occur randomly irrespective of the body size, the probability of a + b is expected to be 2/3 (random probability of mating between heterosize classes), and that of c as 1/3 (that of homosize class). We tested the observed frequency against these expected probabilities using chi-squared tests. These testing procedures were also applied to the SSL trios where the combinations are (a) L-female and S-male, (b) S-female and L-male, and (c) S-female and S-male. Second, we conducted a binomial test of the size-dependent preference for the gender role between L and S combinations by using only data of a and b, with the null hypothesis predicting a ratio of 1:1. If observed body-size combinations in the LS combination were random irrespective of the gender role, there would be an equal mating frequency between a and b.
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RESULTS |
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Experiment 1: relationship between body size and gender role
The variance-ratio test using the F distribution showed that the Kakegawa-DITCH population had a significantly smaller variance than did the other two: F = 4.315, df = 111 and 116, p <.0001 for Kakegawa-POND versus Kakegawa-DITCH; F = 2.631, df = 253 and 116, p <.0001 for Shimizu-DITCH versus Kakegawa-DITCH. Therefore, data for the three populations were analyzed separately (without being pooled).
Figure 1 shows a scatter plot of the body weights of copulated pairs. If more points (the ratio of which is defined as q) are located below the diagonal (y = x), the female role snails are generally larger than are the male role snails. Binomial testing showed that the female role snail was likely to be larger than is the male role snail in a copulated pair (q = 0.80 and p <.05 in Kakegawa-DITCH; q = 0.70 and p <.05 in Kakegawa-POND; q = 0.71 and p <.05 in Shimizu-DITCH).
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The bootstrap test detected a significantly larger mean pairwise difference. The Kakegawa-POND population (p =.017) and the Shimizu-DITCH population (p =.0003) showed a significant difference in the body sizes of a mating pair, whereas the Kakegawa-DITCH population showed a marginally significant difference (p =.052), possibly caused by the reduced variance in the body sizes. Thus, the null hypothesis for experiment 1 was rejected.
Experiment 2: effect of relative body size on gender decisions in pairs of snails
We observed significantly more frequent initial approaches by the male role snails and more rejection behaviors by the female role snails in the LL combination than in the other two (Kruskal-Wallis test, p <.05) (Figure 2A,B). However, the probability of mating (number of successful copulations/total initial approaches in each replicate) was not significantly different between the combinations (Fisher Exact test 
2 = 2.46, df = 2, p =.32) (Figure 2C). The successful copulation rate (number of copulated pairs/total pairs) of SS was lower than the other two combinations (Figure 2D). Small snails played the male role in 66% of the successful LS combination. Both size snails played the male role in the same-size combinations (LL and SS) (Table 1). In the heterosize combination (LS), the small individuals played the male role more frequently than did the large snails did (Table 1). The null hypothesis in experiment 2 was therefore rejected.
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That significantly fewer initial approaches were observed in the wild-type small snails in the SS combination is attributable to several individuals that did not show any initial approach; we do not know why.
Experiment 3: effect of body size on pair formation and gender role among snail trios
The frequency of copulation in the L-female and L-male (LL) pairings was not significantly different from that of the random pairing assumption (1/3) in the LLS combination (2 = 0, df = 1, p = ns) (Table 2). However, the frequency in the S-female and S-male pairings (SS) was significantly less frequent than the random assumption (1/3) in the other trio, SSL (2 = 4.15, df = 1, p <.05). Next, the binomial test was conducted for heterosize combinations (LS and SL). The frequency of L-female and S-male copulations was significantly higher than that of the reverse S-female and L-male pairing, in both triple combinations: p =.0003 in LLS, p <.0001 in SSL.
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These results demonstrate that an initial approach occurs randomly between the two large snails in the LLS trio and that large individuals do not actively avoid the female role. However, the small snails positively played the male role and actively searched for a large partner that would play the female role. On the other hand, in the SSL trio, small individuals avoided the female role, and this is why the frequency of SS copulations was low. Small snails acting as the male actively selected large individuals as females. Because the large snails did not avoid taking the female role, disassortative mating was significantly frequent in this treatment. The null hypothesis for experiment 3 was therefore rejected.
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DISCUSSION |
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Relation between body size and gender role preference
Copulations were likely to occur between snails with a large difference in body weight, and the male role snail was generally smaller than was the female role snail. This result is concordant with the observations on closely related species, P. gyrina and P. heterostropha, reported by DeWitt (1996)
. In the present study, the body size distribution of snails was precisely accounted for in each original field population. Therefore, the bootstrap test, which reflects individual multiple copulations and the body size distribution in a natural population, seems appropriate. DeWitt (1996) tested the body size difference using paired t tests. However, because the same individuals may have joined copulations repeatedly, we preferred to use the bootstrap test, which allows repeated measures. In the present study, snails copulated most readily when large body size differences were seen between partners in all the experiments, in which small ones took the male role and large snails the female role. These results support the gender allocation pattern predicted by the size advantage model. However, in the LL combination, the initial approaches by males were more frequent than in the other two combinations (Table 1 and Figure 2A), and it took more attempts to copulate than in the LS combination, although the probability of successful mating was not significantly different (Figure 2C,D). These results suggest that although large snails are often eager to take the male role, they do not positively refuse to take the female role when the partner is small, or occasionally even not small. Moreover, experiment 3 showed that the individual that takes the male role between large partners in LLS is randomly determined. From the mating patterns of this freshwater snail, if the female role snail accepted initial approaches by the male role snail, they successfully copulated (no gender role swapping in one encounter was observed). If the preferred gender role of large snails is to be female, fewer rejection behavior patterns by the female should have been observed in LL pairs compared with LS pairs. However, LL pairs showed more rejections than did the females in LS pairs. Thus, we conclude that the preferred gender role is the male. When a large snail discovers a partner smaller than itself, it accepts the female role and receives sperm, and when the partner is larger or of similar size, it tries to take the male role to save reproductive energy as the sperm donor.
Why do large snails behave this way (to take both gender roles at equal probability)? Because of their limited mobility, the dynamic changes of individual gender roles will depend on the frequency distribution of individual relative body sizes encountered in a local area. It is unlikely that a large snail will encounter a far larger snail. This makes the expected reproductive success of that large snail very low if it insists on acting in the male role, especially when the population density is low. In that situation, the reproductive success of a snail acting as a female will be higher because producing eggs guarantees reproductive success. Severe sperm competition will enhance the benefit of acting as the female (Angeloni et al., 2002; Charnov, 1996). We suggest that individuals should act as males when small, then as both males and females when larger. Thus, clear gender-role switching associated with body size, which is predicted by the size advantage model, was not seen.
Body size difference between partners as a solution for gender conflict
In experiment 2, members of LL pairs were equally likely to show initial approaches and rejection (Table 1 and Figure 2A,B), which suggests that the preferred gender role is the male. Although we do not say that there is no possibility of their avoiding mechanical injury through copulation (there have been no reports on this in Physa snails), the repeated occurrence of initial approaches and rejections may be explained by the notions of the hermaphroditic dilemma (Leonard, 1990) and gender conflict (Michiels, 1998; Wethington and Dillon, 1996). Gender conflict indicates the conflict of gender decision between the partners in simultaneous hermaphrodites, because both individuals of a pair seek the same gender role. One solution to avoid gender conflict is the well-known egg-trading behavior between two partners in a serranine fish, the black hamlet. This controls the individuals who attempt to cheat by being only sperm donors. Individuals of a pair actively alternate the gender roles in this case (Fischer 1984; see details, Leonard and Lukowiak, 1991; Michiels, 1998). In our experiment, both snails in the LL pairs were eager to act as the male, which may spare the cost of gamete production. This is male-male gender conflict. In contrast, successful copulations in LS pairs occurred after fewer male approaches and fewer female rejections than in LL pairs (Figure 2A,B); however, there was not a significant difference in copulations per initial approach (Figure 2C). Thus, size differences between the paired snails are another solution for resolving gender conflict.
Why are small snails likely to play the male role?
P. acuta continues to grow even after sexual maturation and thus needs to allocate its resources simultaneously to growth and reproduction (Sterns, 1992). Small snails must allocate resources to both, whereas large snails allocate more to reproduction. It may thus be advantageous for the small individuals to play the male role, in which it is less costly to produce gametes. When individuals become large enough, they do not need to invest as many resources for growth. Thereafter, the resource is converted to gamete production, and thus, both gender roles may be acceptable in large snails. Another possibility is that the relative advantage of making eggs will be high enough to be a net benefit (relative to making sperm) when an individual attains a certain size even though less energy is required to produce sperm than to produce eggs.
To examine these two hypotheses, we are preparing another study describing the relationships between the body size and lifetime fecundity associated with the tradeoffs between reproduction and growth. It would be worthwhile to examine how gender decision making in relation to body size affects fitness in simultaneous hermaphrodites.
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ACKNOWLEDGEMENTS |
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We thank T.J. DeWitt for helpful comments on an earlier manuscript version, E. Kasuya for advising statistical method, S. Katada and Y. Hodoki for helpful comments on manuscript and valuable discussions, H. Kurota for collecting snails in the field, and A. Houde and anonymous reviewers for valuable comments on the manuscript. This research was partly supported by the JSPS Research Fellowships for Young Scientists, and a Grant-in-Aid for Encouragement of Young Scientists from MESC (NO.11–09822) to K.O. and a Grant-in-Aid for Scientific Research from MESC (NO 12440215) to M.S.
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