Biol. Bull. 215: 126-134. (October 2008)
© 2008 Marine Biological Laboratory
Phenotypic Plasticity and Sexual Dimorphism in Size at Post-Juvenile Metamorphosis: Common-Garden Rearing of an Intertidal Gastropod With Determinate Growth
Takahiro Irie* and
Naoko Morimoto
Sesoko Station, Tropical Biosphere Research Center, University of the Ryukyus, 3422 Sesoko, Motobu, Okinawa 905-0227, Japan
* To whom correspondence should be addressed. E-mail: irie{at}bio-math10.biology.kyushu-u.ac.jp
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Abstract
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Proximate factors of the intraspecific variation in molluscan shell morphology have long received attention in biology. The intertidal gastropod Monetaria annulus (Mollusca; Gastropoda; Cypraeidae) is particularly suitable for the study of variation in body size, because this species is a determinate grower in the sense that soft-body size shows no further increase after the juvenile stage. Cross-sectional field surveys on post-juvenile individuals have indicated that the mean body size varies widely among populations and is larger in females than in males within populations. To examine whether these patterns are due to genetic differences, we conducted a common-garden rearing experiment with juvenile individuals collected from two populations on Okinawa Island. After adjusting for among-individual differences in initial degree of development, statistical analyses revealed that this species exhibits female-biased sexual size dimorphism mediated by a longer development time rather than by faster growth rates in females. Although wild individuals show a remarkable size difference between populations, no size difference was found between the populations in the individuals reared in a common-garden condition. This result suggests that the among-population size difference does not have a genetic basis and is caused by phenotypic plasticity based on environmental heterogeneity among habitats.
Abbreviations: DD, degree of development • DTM, days to metamorphosis • IDD, initial degree of development • IW, initial shell width • JW, juvenile shell width at metamorphosis • LGR, linear growth rate • NJW, native juvenile shell width • SSD, sexual size dimorphism
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Introduction
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It has long been recognized that marine gastropods show remarkable geographic variations in shell morphology (Vermeij, 1972; Reid, 1996). For taxonomists, the question of whether these variations reflect genetic differences is important because genetically driven variations might be used as a clue for morphological taxonomy (e.g., Phillips et al., 1973; Tissot, 1984). Ecologists also have paid attention to geographic patterns in shell thickness due to inducible responses to predators or prey (e.g., Boulding and Van Alstyne, 1993; Trussell, 2000a, b) and to other morphological traits (Padilla, 1998). Evaluation of the genetic and environmental influences on phenotypic variation observed in the field is an inevitable process in these studies. A standard method for this evaluation is the common-garden experiment, in which the offspring of individuals from different populations are reared in a common environment to control for environmental influences on phenotypic traits (Conover and Schultz, 1995; Fairbairn et al., 2007).
Intraspecific variation in body size at a transition between ontogenetic stages (i.e., metamorphosis or sexual maturity) is a frequent focus in life-history studies (e.g., Day and Rowe, 2002). Invertebrates often exhibit female-biased sexual size dimorphism (SSD)—that is, females mature at a larger size than males (e.g., Gilbert and Williamson, 1983; Andersson, 1994; Fairbairn, 1997; Maly and Maly, 1999; Blanckenhorn et al., 2007). Variation in adult size among populations is also common in various taxa and often reflects spatial variation in size at maturity in determinate growers (organisms with no further somatic growth after sexual maturation; Kozlowski and Wiegert, 1987). When all other factors are equal (e.g., initial size), a sexual difference in transition size (i.e., size at metamorphosis or maturity) results from sex-based differences in development time, somatic growth rates, or both. It is important to elucidate whether larger body sizes are the consequence of longer development or faster growth, because this distinction may help reveal the ecological and evolutionary origins of the variation in body size.
Size at a transition, development time, and growth rates are plastic traits in many organisms, and they sometimes respond to the environmental conditions experienced during ontogeny with delay or through cumulative action. Biologists have recognized several types of non-instantaneous plasticity in these traits: cross-generation effects such as maternal effects (Mousseau, 1991), developmental switches (Scheiner, 1993), developmental inertia (Bradshaw and Johnson, 1995), and effects of growth history (Arnett and Gotelli, 1999). In the possible presence of such plasticity, common-garden experiments across generations are ideal (Palmer, 1985, 1994; Parsons, 1997), but experiments with only a single generation of wild-caught individuals are often conducted in those species for which intergenerational rearing has not been successful (Martín-Mora et al., 1995; Johnson and Black, 1998; Trussell, 2000a, b; Delgado et al., 2002; Smith and Ruiz, 2004; Kurihara et al., 2006). However, unless researchers can rule out or adjust for the possible effect of such plasticity, within-generation experiments may be insufficient to evaluate the genetic basis of the focal phenotypic variation. This occurs because one cannot distinguish whether it is difference in genotype or in past environments that is responsible for the phenotypic differences observed in a common rearing environment. The same holds true for reciprocal transplant experiments, in which individuals derived from different populations are released together in each of the original habitats (see Discussion).
Among benthic marine species, cowries (Gastropoda; Cypraeidae) are particularly suitable for the study of adult body size because they exhibit explicit determinate growth, which makes it easy to quantify body size at the onset of the adult stage. Veliger hatchlings spend a certain period in a planktonic stage and then settle in the benthic habitat after the first metamorphosis. The benthic life-history of cowries consists of three stages: juvenile, callus-building, and adult (Fig. 1). During the juvenile stage, cowries increase their soft-body volume while forming a coiled, fragile shell. At the end of the juvenile stage, cowries experience a second metamorphosis (hereinafter simply referred to as metamorphosis), in which the shell coiling stops and the shell aperture narrows. In the next stage, calcareous material is deposited on both the lateral exterior and dorsal interior surfaces of the shell constructed during the juvenile stage (referred to as the juvenile shell) to thicken a "callus" that appears to serve as a defense against predators (see Fig. 1). Cowries are explicit determinate growers in the sense that the size of a juvenile shell (and the volume of the soft body) does not increase after the juvenile stage. Reproduction begins after the end of the callus-building stage.
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Figure 1. An ontogenetic series of Monetaria annulus (upper row: dorsal view; lower row: anterior view). Shell size was measured as initial shell width (IW) at the beginning of rearing and juvenile shell width at metamorphosis (JW).
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The gold-ringed cowry Monetaria annulus (Linnaeus, 1759) is abundant on intertidal shores with a variety of substrata across the Indo-Pacific tropics and subtropics. This species is dioecious and has no sex change. Internal fertilization occurs after a male inserts his penis into a female body during copulation. We consider that this species is polyandrous because there is no evidence that a female mates with only a particular male. Females protect an egg mass laid on the surface of rocks or algae by mounting it for a certain period. Juvenile individuals and brooding females are found throughout the year in Okinawa Island, Japan (Katoh, 1989), and thus generations overlap considerably.
Comparison among randomly collected post-juvenile individuals has revealed that mean body size is larger in females than in males within populations (Irie and Adams, 2007). This pattern probably reflects female-biased SSD. However, one cannot rule out the possibility that there is no sexual difference in size at metamorphosis and that post-juvenile demographic processes are instead responsible for the SSD (e.g., larger females live longer than smaller ones, but male survival is independent of size).
Independent of SSD, among-population variation in shell size at metamorphosis has been reported in many cypraeid species (Kay, 1961; Schilder, 1961; Wilson and Summers, 1966; Renaud, 1976; Tissot, 1984; Irie and Iwasa, 2003). Randomly collected post-metamorphic individuals of Monetaria annulus exhibit remarkable variation in juvenile shell size within and among neighboring populations (Orr, 1959); on Okinawa, individuals are smaller in more sheltered habitats (Irie, 2006; Irie and Adams, 2007). It has been unclear whether the substantial size variation evident in this species is genetically driven or the result of plastic responses to local environmental conditions.
No one has succeeded in rearing the planktonic larvae of Monetaria annulus to settlement. In the present study, therefore, we reared in the laboratory wild-grown juvenile individuals collected from two Okinawan populations, aiming to evaluate the phenotypic responses of size at metamorphosis, juvenile period, and juvenile growth rates in a common environment. In particular, we were interested in (1) whether females metamorphose at a larger size than males, (2) whether the female-biased SSD is accompanied by longer development or faster growth in females, and (3) whether the among-population size variation is based on genetic differences.
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Materials and Methods
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Common-garden rearing experiment
In November 2006, 40 juvenile individuals were collected from intertidal benches at the Yamada and Sesoko coasts of Okinawa Island (see Irie, 2006). These populations are about 25 km apart and differ in terms of the size of their post-juvenile cowries: juvenile shell size at metamorphosis is considerably larger in Sesoko than in Yamada (Irie, 2006; Irie and Adams, 2007).
Collected cowries were placed singly in plastic bottles containing seawater and carried to the Sesoko Station within a few hours. Prior to the experiment, the cowries were photographed to measure the initial shell width (IW; Fig. 1), and then assigned individually to plastic cuboid bottles (6 cm x 6 cm x 13 cm depth) capped with polyester lids with a 1-mm mesh. The bottles were placed in a large plastic tank (length, 85 cm; width, 58 cm; depth, 20 cm).
Fresh seawater that was continuously pumped from a depth of several meters in front of the research station was independently forced into each bottle at a rate of 100 ml min–1 through plastic tubes (inner diameter, 3 mm) by a small pump fixed at the bottom of a watershed tank. Waste seawater overflowing from each bottle was drained and did not flow into any of the other bottles in this system. To equalize the rearing conditions, bottles in the tank were haphazardly rearranged every day, and the temperature was controlled by both electric coolers (1200 W) and heaters (4500 W) with thermostats placed in the watershed tank with continuous aeration. The water temperature of the tanks was recorded hourly by digital data loggers (Thermochron: DS1921G-F50) throughout the experiments. Experiments were conducted in a room with north-facing windows and no artificial light sources.
Both juveniles and adults of this species feed on algae attached on the substrate. To provide food far in excess of consumption, we cultured in the laboratory an algal bed mainly consisting of green algae on the surface of limestone fragments spread over the bottom of large tanks. To accelerate algal growth, we added Hyponex all-purpose liquid fertilizer (6-10-5; Hyponex Japan Corp., Ltd., Osaka, Japan) to the flowing seawater in the closed-system tanks every 2 days (concentration: 100 ppm). All the bottles were cleaned, and any grazed limestone fragments were replaced with a fresh crop of algae every afternoon. This procedure made it possible to rear cowries with no food limitation.
During the juvenile stage, cowries spirally enlarge a fragile shell. Near the end of the juvenile stage, cowries dome the final shell whorl upward and eventually narrow the shell aperture by turning the outer lip inward. We defined the final day of the juvenile stage (= the date of metamorphosis) as the date when the final outer lip was constructed, and the days to metamorphosis (DTM) as the number of days from the onset of rearing to metamorphosis (Fig. 2). Using digital calipers, we measured the juvenile shell width only twice, once at the beginning of the experiment (initial width: IW) and again at the end of the juvenile stage (juvenile width at metamorphosis: JW; Fig. 1). Our measurements of body size were designed to minimize handling of juveniles, which damages the shell lip and may lower the growth rate.
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Figure 2. Ontogenetic increase in shell width of a juvenile individual when it grows in a wild population (dashed curve) and when it is reared in the laboratory (solid curve) until metamorphosis. DTM is the number of days from the onset of rearing to metamorphosis. Left and right endpoints of the solid curve indicate the shell width at the beginning of rearing (IW) and the shell width at metamorphosis (JW), respectively. Native juvenile shell width at metamorphosis (NJW) is the metamorphic size to which the individual in a wild population grows to metamorphosis. Initial degree of development (IDD) is defined as IW/NJW. Laboratory conditions induce slower growth, but have no effect on development time in this hypothetical example.
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Linear growth rate (LGR) was defined as the mean increment of juvenile shell width per day and was calculated as (JW – IW)/DTM. Since the growth of juvenile shell size follows a sigmoid curve in Monetaria annulus (Katoh, 1989), comparison of LGR among individuals is meaningless unless adjusted for the variation in initial degree of development (see "Estimation of initial degree of development").
The external shell was broken, and the sex of each individual was anatomically determined after the conclusion of the experiment, because living cowries cannot be sexed without dissection.
Estimation of initial degree of development
Initial shell width (IW) was variable among individuals. In the presence of SSD, it is obviously erroneous to compare trait values (JW, DTM, LGR) between the males and females by including IW as a covariate, because the same IW does not mean the same developmental status between the sexes. The same can be said for the among-population size difference. Thus, we defined degree of development (DD) as the proportion of juvenile shell size to size at metamorphosis; this quantity continues to increase from a small value to unity during the juvenile stage (Fig. 2). Initial degree of development (IDD), defined as DD at the beginning of rearing, was calculated as initial shell width divided by native juvenile shell width at metamorphosis (i.e., IDD = IW/NJW), where NJW is the estimated shell width at metamorphosis for the individuals that stay in the wild population until metamorphosis (Fig. 3). IDD was incorporated into general linear models as a covariate to adjust the variation in initial developmental stage among individuals (see "Statistical analysis").
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Figure 3. Estimation of native size at metamorphosis (NJW), or expected shell width at metamorphosis for the individuals who stay in the wild population until metamorphosis. Solid line is a regression line calculated from juvenile shell width at metamorphosis (JW) plotted against initial shell width (IW) measured from the reared individuals (dots). Because IW and JW are equal on the dashed line (i.e., the diagonal line fulfilling Y = X), the intersection point of the two lines indicates the expected NJW. NJW for each individual was Eq. 4 by adding the corresponding residual from the regression line to the expected NJW (see Eq. 4). Data for males from Yamada (n = 21) are shown in this figure. NJW for females from Yamada and for individuals from Sesoko were estimated in the same way.
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NJW of each individual was estimated in the manner described below (see also Fig. 3). First of all, IW and JW measured from reared individuals are related by an equation:
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where a is the slope and b is the y-intercept of the regression line. Because NJW is equivalent to the expected IW of the individuals that metamorphosed immediately after the rearing started, we have
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where E(NJW) denotes the expected value of NJW. Accordingly, E(NJW) is given by substituting IW and JW in Eq. 1 with E(NJW) in Eq. 2 and then solving it for E(NJW):
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Because NJW of each individual is (normally) distributed around the mean, E(NJW), NJW of the i-th individual can be calculated as
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where Ri is the residual for the i-th individual from the regression line given by Eq. 1.
Since the expected NJW should differ between the sexes and among derived populations (see "Introduction"), the coefficients a and b in Eq. 3 must take different values among the combinations of sex and population. We thus applied a general linear model to the data, in which JW was the response variable and Sex (male or female), Population (Yamada or Sesoko), IW (covariate), and their interactions were explanatory variables (Table 1). Because all interaction terms involving the covariate were found to be nonsignificant (Table 1), we removed these terms from the model to avoid reducing the estimation accuracy due to small sample size. We subsequently estimated the common slope (a) across and the y-intercepts (b values) of the regression lines for all combinations of Sex and Population. Finally, NJW for all individuals was calculated from Eq. 4.
Statistical analysis
We first analyzed JW, DTM, and LGR using MANCOVA with Sex (male or female), Population (Yamada or Sesoko), and IDD (covariate) and their interactions as explanatory variables and then conducted univariate ANCOVA on each dependent variable, in which nonsignificant interactions with the covariate were pooled with the error term in the final analyses. Since analyses on DTM and LGR found regression slopes to be heterogeneous between the derived populations, we used the Johnson-Neyman procedure (
= 0.05) to identify those covariate ranges in which Population effect was significant (Huitema, 1980). We omitted from these analyses two individuals that died during the experiment because of a manipulative mistake and two individuals with malformed shells. JMP statistical software (ver. 5.1.2 for Windows NT, SAS Institute) and Mathematica (ver. 5.2 for Windows, Wolfram Research) were used to conduct statistical analyses.
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Results
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The multivariate analysis found significant effects of Sex, Population, and initial degree of development (IDD) as well as significant Population-by-IDD interaction (Table 2A). Univariate analysis on juvenile shell width at metamorphosis (JW) indicated that none of the interactions were significant (Table 2B) and larger IDD led to significantly larger JW. Females metamorphosed at significantly larger size than males (Table 2B; Fig. 4A), and the between-population difference was nonsignificant (Fig. 4A). Females spent more time before metamorphosis (Fig. 4B), and individuals with lower IDD had longer days to metamorphosis (DTM) regardless of Sex and Population (Table 2B). Population-by-IDD interaction was significant (Table 2B), and the Johnson-Neyman procedure indicated that the Population effect on DTM was nonsignificant if IDD fell below a threshold value (males, IDD < 0.440; females, IDD < 0.418; see Fig. 4D); otherwise, DTM was significantly longer in the individuals from Sesoko than in those from Yamada. No statistically significant sexual difference was found in linear growth rate (LGR) (Table 2B; Fig. 4C). LGR did not differ between populations if an individual's IDD fell below a threshold value (males, IDD < 0.458; females, IDD < 0.355; see Fig. 4E); otherwise, LGR was significantly greater in the individuals from Yamada than in those from Sesoko.
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Figure 4. Covariate-adjusted means (at the grand mean, initial degree of development [IDD] = 0.409) and standard errors for (A) juvenile shell width (JW), (B) days to metamorphosis (DTM), and (C) linear growth rate (LGR) calculated from all the individuals according to the final models. Results of the Johnson-Neyman analyses for (D) DTM and (E) LGR were summarized with adjusted means (at the IDD grand means across populations) and standard errors calculated from the individuals that fell below the threshold values (see Results). See panels (B) and (C) for the between-sex patterns in DTM and LGR, because the threshold values and covariate grand means used in panels (D) and (E) are different between the sexes and thus inappropriate for between-sex comparisons.
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Discussion
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Proximate factors of intraspecific variation in size at a life-history transition have been less investigated in marine molluscs, particularly in contrast to the situation in terrestrial organisms. In the present study, we obtained clear results on whether the among-population and sex-based differences in size at post-juvenile metamorphosis have a genetic basis, by rearing wild-caught juvenile Monetaria annulus in a common environment.
Between-population patterns
In the present study, we found no evidence that the among-population size difference in the field has a genetic basis. This result is consistent with the predictions in many previous papers (Orr, 1959; Tissot, 1984; Irie, 2006), in which authors pointed out that, at least at a microgeographic scale, genetic differentiation among populations is not an appealing explanation when considering the species’ high dispersal potential during the planktonic stage and the resultant strong gene flow in intertidal cowries. Thus, the size variation among populations is probably caused by phenotypic plasticity in response to the geographic difference in environmental conditions. In fact, our experiment demonstrates that size at metamorphosis is a plastic trait in Monetaria annulus by showing that this trait strongly depends on the initial degree of development. However, further studies are required to determine whether this conclusion can be extended to the range-wide patterns, such as size variation across latitude (reported by Irie, 2006).
We observed a positive relationship between initial degree of development and size at metamorphosis. This suggests that rearing tanks created environmental conditions that induce smaller size at metamorphosis compared to the wild populations, because individuals that were less developed initially were exposed to laboratory conditions for a longer time. In fact, regardless of the initial degree of development, size at metamorphosis of reared individuals was smaller than that of wild-grown individuals (Table 3). It would be difficult, however, to identify which environmental factors are responsible for the size difference between wild-grown and laboratory-reared individuals, because ectotherms alter their transition size in response to various environmental factors (Berrigan and Charnov, 1994; Nylin and Gotthard, 1998), including temperature (Atkinson, 1996), food availability (Arnett and Gotelli, 1999), photoperiod (Masaki, 1972; De Block and Stoks, 2003), and predators’ effluent (Benard, 2004).
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Table 3 Comparison of shell width at metamorphosis (JW) between laboratory-reared and wild-grown Monetaria annulus
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Observed growth rate differences between populations seem to be better explained by the plasticity in physiological traits known as acclimation (sensu Huey and Berrigan, 1996) rather than by genetic differences between populations. The population-level difference was remarkable in those individuals that were close to metamorphosis at the beginning of rearing, but was absent in individuals that were initially less developed (Fig. 4E). This pattern suggests that juvenile cowries may exhibit similar growth rates in a common environment independent of derived populations, but the growth rate response to altered environments is accompanied by a time delay. These conjectures have to be confirmed by better-designed experiments in the future, because our experiment cannot rigorously rule out the possibility that phenotypic differences between populations are based on genotype-by-environment interactions.
Between-sex patterns
The common-garden experiment in this study confirmed that the gold-ringed cowry shows female-biased sexual size dimorphism (SSD) (Fig. 4A). Irie and Adams (2007) identified SSD in this species by comparing between the sexes the mean body sizes of post-juvenile individuals randomly collected from wild populations. Rigorously speaking, however, such a cross-sectional survey cannot rule out the possibility that a sex-based difference in the size-dependence of adult mortality is responsible for the apparent size dimorphism. In contrast, by comparing size at metamorphosis between males and females grown in the same environment, the present study provides a conclusive demonstration that the female-biased SSD is a "true" pattern.
In the gold-ringed cowry, evolutionary forces selecting for larger female size may be twofold. First, female fecundity typically increases with body size (size-fecundity advantage; Charnov, 1982; Howard, 1988; Shine, 1988; Honek, 1993; Preziosi et al., 1996); indeed, this species shows a positive relationship between body size and egg mass size (Katoh, 1989). Second, larger females may ensure greater parental care by protecting deposited eggs for a longer time, because larger adult size often leads to greater resistance against starvation (e.g., Peters, 1983; Calder, 1984) and predation (i.e., size-refuge; e.g., Crowl and Covich, 1990).
Our results suggest that a sex-based difference in juvenile period, not juvenile growth rates, leads to female-biased SSD in the gold-ringed cowry (Fig. 4C). In the holometabolous insects with a shorter development time in males (i.e., protandry), female-biased SDD is often explained as a by-product of sexual selection arising from sperm competition, because protandrous males can maximize their reproductive success by increasing the likelihood of copulating with virgin females (Wiklund and Fagerström, 1977; Fagerström and Wiklund, 1982; Iwasa et al., 1983). However, sexual selection favoring early male emergence may not be important as a driving force of female-biased SSD in the gold-ringed cowry, because the polyandry and severe generation overlap in this species is predicted to work against its evolution (Wiklund and Fagerström, 1977; Fagerström and Wiklund, 1982; Singer, 1982; Bulmer, 1983; Iwasa et al., 1983; Iwasa and Haccou, 1994).
Feasibility of reciprocal transplants
Along with common-garden experiments, reciprocal transplants are often used to evaluate the genetic and environmental effects on phenotypic variations between populations. Reciprocal transplants might be better suited for answering the questions addressed in the present study, because effects of environmental conditions on phenotypes should be less artificial than those in a laboratory common-garden. On the other hand, the approach has a great disadvantage in that the individuals that are not recaptured after experiments may alter the natural distribution of genotypes, which obstructs further examinations in the same area (Conover and Schultz, 1995).
Application of reciprocal transplants to the gold-ringed cowry is much harder than expected. Enclosures containing animals are often placed at their habitats in insects (e.g., Arnett and Gotelli, 1999; Fordyce and Nice, 2004), reptiles (e.g., Niewiarowski and Roosenburg, 1993), and even in intertidal gastropods (Trussell, 2000b), but such a method is not feasible on reef-flats not only because the environments inside cages significantly differ from the outside by trapping silts, but also because occasional storms easily dislodge cages from substrates. Difficulties will still remain even if tagged individuals are released, instead. Experimenters have to check whether each individual has metamorphosed every few days to quantify days to metamorphosis (and thus linear growth rates), because these variables cannot be back-estimated from mature individuals. Considering that habitats of the gold-ringed cowry are exposed only during spring low tides, reciprocal transplants may not be workable in this species.
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Acknowledgments
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The authors thank W. F. Fagan, M. LaBarbera, G. J. Vermeij, and an anonymous reviewer for commenting on the manuscript. T. Asami, Y. Iwasa, O. Kishida, K. Sakai, G. C. Trussell, M. Yamaguchi, and K. Yamahira also made valuable suggestions that improved the manuscript. This study was assisted by S. Nakamura and Y. Nakano at Sesoko Station, Tropical Biosphere Research Center. This project was funded by the Japan Society for the Promotion of Science (JSPS).
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Footnotes
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Received 7 January 2008; accepted 4 April 2008.
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Abstract
Introduction
