Behavioral Ecology Advance Access originally published online on October 12, 2005
Behavioral Ecology 2006 17(1):1-5; doi:10.1093/beheco/ari093
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How outcrossing hermaphrodites sense the presence of conspecifics and suppress female allocation
a SchleicherováDepartment of Animal and Human Biology, University of Turin, Via Accademia Albertina 13, 10123 Turin, Italy
Address correspondence to M.C. Lorenzi. E-mail: cristina.lorenzi{at}unito.it.
Received 13 March 2005; revised 2 June 2005; accepted 4 July 2005.
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ABSTRACT |
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One of the greatest remaining problems in the field of sex allocation is the variation across species of the extent to which individuals adjust their offspring sex ratio or sex allocation according to environmental conditions. Particularly in the field of sex allocation, there is a lack of research on the mechanisms and cues involved. We address this problem in the outcrossing simultaneous hermaphroditic polychaete Ophryotrocha diadema, which shifts sex allocation by suppressing the female function in the presence of reproductive competitors or multiple partners. We document that O. diadema hermaphrodites can evaluate group size by means of a species-specific chemical released by mature individuals in water. The perception of such a water-borne signal is sufficient to trigger the observed shift in sex allocation, i.e., a suppression of the female function, irrespective of the frequency of encounters with conspecifics. Under natural conditions, such a pheromone will favor partners' encounters and the adjustment of individual sex allocation according to the numbers of reproductive competitors and/or potential partners.
Key words: adjustment, assessment, chemical cues, perceptual abilities, polychaetes, sex allocation.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Sex allocation theory assumes that hermaphrodites allocate a limited amount of resources to reproduction divided between sperm and eggs. In the simplest models, the fraction devoted to the male function depends only on the mating group size, k + 1, where k is the number of reproductive competitors (Charnov, 1982
; Fischer, 1984). In outcrossing hermaphrodites forming monogamous pairs, k = 1. In this situation, both partners are expected to allocate as few resources as possible to sperm production (the minimum amount of sperm to fertilize the partner's eggs). All the remaining resources are expected to be diverted to egg production. As the number of reproductive competitors or potential partners increases, the allocation to the male function is expected to increase and allocation to the female function to decrease, approaching one-half of the total amount of reproductive resources. The resulting sex allocation (i.e., the proportion of resources allocated to the male functions) is appropriate to the social condition encountered.
This prediction relies on the assumption that hermaphrodites respond to group size and adjust their sexual investment accordingly. Also gonochorists, under local mate competition (Hamilton, 1967), adjust their offspring sex ratio according to the number of fertilized females in the local group. Gonochorists have to choose the optimal sex ratio for their offspring when they become sexually mature without knowing what environment they will meet. Hermaphrodites can simply choose to invest in the gender that yields the highest immediate success. But both gonochorists and hermaphrodites are selected to detect in the surrounding environment the information useful for adaptive adjustment of their reproductive investments. It has been suggested that the ability of organisms to assess relevant cues about their environment may be a major factor constraining the extent to which individuals adaptively adjust sex allocation (West and Sheldon, 2002). However, despite their fundamental importance, very few studies have investigated the cues, of whatever nature, that individuals use to assess relevant factors about their environment (Keller, 2004; Shuker and West, 2004), and in particular, none have investigated hermaphrodites' cues.
We know that chemical cues are used in reproduction by various aquatic animals. In fish, pheromones regulate interactions between mating individuals. Some of the chemical cues are produced by males and perceived by other male competitors (Stacey et al., 2003). In some hermaphroditic gastropods, a chemical produced by an individual is injected into another with a love dart, and it "manipulates" the recipient's reproductive conditions (Helix aspersa, Koene and Chase, 1998). In Aplysia californica, a water-borne, long-distance peptide pheromone deposited on the surface of the egg-ribbon attracts mates (Painter et al., 2004). Among polychaete worms, the study of chemical signals related to reproduction revealed the existence of species-specific sex pheromones in a few species (reviewed by Andries, 2001). In the sequential hermaphrodite Ophryotrocha puerilis, water-borne pheromones produced by females attract males (Berglund, 1990), and the "pair culture effect" (resulting from the fact that placing two mature females together causes one of the two to change sex, Hartmann and Huth, 1936) is induced by a lipidic pheromone (Marchionni and Rolando, 1981).
There is increasing evidence that hermaphrodites adjust their sex allocation on the basis of social conditions (Lorenzi, et al., in press; Raimondi and Martin, 1991; Schärer and Ladurner, 2003; Schärer et al., 2005; Trouvé et al., 1999) and partner state (Anthes and Michiels, 2005; Koene and Ter Maat, 2005). However, no paper, to our knowledge, has addressed the question of the cues that hermaphrodites use to assess their social environment, although simple decision-making mechanisms are expected.
The hermaphroditic polychaete worm Ophryotrocha diadema is an excellent model system to test the mechanisms underlying sex allocation adjustment. In this species, reciprocal egg fertilization occurs by regular alternation of sexual roles within the mating pair and results in balanced male and female reproductive success. In these conditions, individuals produce large numbers of eggs and as few sperm as they need to fertilize their partner's eggs (Sella, 1985). Under more dense social conditions, O. diadema hermaphrodites diminish their female allocation, in favor of the male sex, to respond to the sperm competition caused by the presence of rivals and by the enhanced mating opportunities (Lorenzi et al., in press). However, the resources subtracted from the female function are not entirely shifted to sperm production but probably also to other aspects of the male function (e.g., direct competition with rivals for fertilization) (Lorenzi MC, personal communication), and they do not affect the growth of mature hermaphrodites (Lorenzi et al., in press). In this species, variations in sex allocation are not caused by density, crowding, or metabolite accumulation but exclusively by the perception of the number of conspecifics (Lorenzi et al., in press). Thus, this ability is crucial to adaptive sex allocation.
Here we first experimentally manipulated the group size of mature hermaphrodites of O. diadema to test for the ability of these polychaete worms to evaluate different numbers of potential partners or reproductive competitors. Then we verified whether they use chemicals, physical interference, or energy expenditure as cues for the estimation of the number of conspecifics and whether cues are species specific. We also investigated which is the origin of the identified cues. Our experiments also throw light on the question whether the observed variations in sex allocation according to social conditions are the consequence of an increase in male expenditure when hermaphrodites mate more often just because they meet more partners or whether they are the expression of an adaptive decision-making process.
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METHODS |
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Study animal
Populations of O. diadema were found among the fouling fauna of Californian harbors by Åkesson (1976)
and Reish DJ (personal communication). According to Reish, such populations are at low density. However, adults live in a network of mucous trails that can be followed by conspecifics, probably leading to a patchy distribution. The life cycle consists of a protandrous phase, followed by a simultaneously hermaphroditic phase which starts when individuals are 14- to 15-segments long (Åkesson, 1982) and last for 30–40 days approximately. Mating is preceded by a 4- to 5-h-long courtship, during which both partners rub mutually against each other, and is achieved by pseudocopulation, a process of external fertilization in which partners maintain a close physical contact before releasing their gametes. Partners regularly alternate sexual roles by reciprocally exchanging a cocoon with 20–25 eggs every 2 days (Sella, 1985). Cocoons are transparent, and egg development can be followed under a stereomicroscope.
Mass cultures of O. diadema are reared according to Åkesson (1976). For this experiment, we used animals derived from laboratory strains established in 1980 and renewed in 1995 and 2001.
All the hermaphrodites used in experiments were virgin, 14- to 15-segments long, and of the same age. To avoid pseudoreplication, care was taken to avoid putting siblings together in the same bowl and in the same treatment group. Experiments were performed in 10-ml bowls, and food was always given in excess.
To check the species specificity of chemical cues, the simultaneous hermaphrodite Ophryotrocha hartmanni was used as a control. The two species are not sympatric: while O. diadema occurs along the Californian coast, O. hartmanni can be found along the Mediterranean and European Atlantic coasts (Åkesson, 1973); however, the two species show similar reproductive behavior (Sella and Ramella, 1999).
Experimental design
Before testing whether O. diadema is able to assess the number of competitors, we checked whether regular water change affects egg production in pairs reared in 10-ml bowls. In a 9-day period, we counted the number of eggs and cocoons produced by hermaphrodite pairs which had their water changed daily (n = 33 replicates) (per pair mean number of cocoons and eggs: 5.97 ± 0.63 and 267.33 ± 52.49, respectively) or only once in 9 days (on day 6) (n = 33 replicates) (per pair cocoons and eggs: 5.85 ± 0.57 and 306.09 ± 125.73, respectively). Egg and cocoon production did not differ (Mann-Whitney U test—for cocoons: U = 516.5, p = .67; for eggs: U = 502, p = .59). This result documents that changing water daily or after 6 days does not affect egg or cocoon production in paired hermaphrodites reared in our experimental conditions.
In the following experiments, food was always given in excess in order to avoid competition for food, although this may make a trade-off less visible as an increase in one sex function can be compensated for by eating more rather than by reducing the other sex function.
Group size assessment
To test whether female allocation varies as a function of group size, we set up three parallel groups, with 2, 6, and 12 mature hermaphrodites per bowl. For pairs and medium groups (6 individuals) we had 33 replicates, for large groups (12 individuals), 30. We expected that if worms perceive the number of reproductive competitors and/or partners precisely, they must adjust their sex allocation accordingly.
To control for consistent water quality across group sizes, we changed water in the bowls with pairs once in every 6 days, every 2 days in medium, and daily in large groups, so that each worm received on average 0.85 ml of fresh sea water daily. This schedule does not control for possible daily fluctuations in water quality but guarantees comparable amount of fresh water to the tested individuals.
Bowls were checked daily for 9 days because in previous experiments this time interval proved to be long enough to detect variations in sex allocation (Lorenzi et al., in press); each time we noted the number of newly laid cocoons and the number of eggs per cocoon. Allocation to the female function was measured as the mean number of cocoons and eggs per pair in each of the three groups.
Data on female allocation were obtained from 33 replicates from the pairs, 31 from the medium, and 26 from the large groups. The other replicates were discarded because some individuals died (mortality rates did not differ between groups, G test, G = 5.91, df = 2, ns).
Relevance of chemical cues and their species specificity
To test whether the chemical cues potentially used by O. diadema hermaphrodites to evaluate the group size were species-specific chemicals, we designed the following experiment by using the congeneric nonsympatric species, O. hartmanni, which is also a pair mating simultaneous hermaphrodite. Individuals of O. hartmanni are reared in the same conditions (temperature and salinity) as O. diadema (Åkesson, 1973), eat the same food, and have the same size.
We first produced conditioned water. The day before the beginning of the experiment, we set up bowls with 12 nonsibling mature O. diadema hermaphrodites which were designed to produce conspecific-conditioned water (36 replicates) and bowls with 12 nonsibling mature O. hartmanni hermaphrodites which were designed to produce heterospecific-conditioned water (36 replicates). To obtain water containing the supposed chemical cue (conditioned water), the water of the bowls was changed daily for 9 days. Each day the removed water was collected in a beaker and immediately used for the conditioned-water treatment. Both conspecific- and heterospecific-conditioned water was collected daily and transferred to two experimental groups in the following way. (1) Conspecific conditioned–water treatment: Pairs of virgin, 14- to 15-segment-long hermaphrodites were set up in clean bowls. Every day the water in the bowl was removed, and they received 10 ml water from O. diadema bowls (36 replicates). (2) Heterospecific conditioned–water treatment: As above, but hermaphrodites received 10 ml water from O. hartmanni bowls daily (36 replicates). (3) Control treatment: Pairs of virgin, 14- to 15-segments-long hermaphrodites were set up in clean bowls with pure water (which was changed with other pure water on day 6 as we previously showed that changing water daily or after 6 days does not affect egg or cocoon production in paired individuals).
The whole experiment lasted 9 days, and bowls were checked every day. We noted the number of newly laid egg-cocoons and the number of eggs per cocoon. Allocation to the female function was measured as the mean number of cocoons and eggs per pair.
Origin of cues: water-borne versus trail-borne cues
O. diadema hermaphrodites might produce a chemical signal that they could release directly in water, in their mucous trails, or in the cocoon matrix. To test this possibility, we checked whether pairs of mature individuals reared in water containing the supposed chemical signal (conditioned-water pairs) or put in bowls containing mucous trails (mucous-trail pairs) reduced their egg production compared to pairs reared in pure water (control pairs).
Production of bowls with mucous trails
To obtain mucous trails before the beginning of the experiment, 30 bowls with 12 hermaphrodites each were set up and left undisturbed for 7 days, so that hermaphrodites could build a rich system of mucous trails along the walls of the bowls. Then both water and hermaphrodites were removed, and the bowls were immediately used for mucous-trail treatment.
Production of conditioned water
As in the previous experiment, we also produced conditioned water by setting another 30 10-ml bowls with 12 mature hermaphrodites the day before the beginning of the experiment.
Procedure
We simultaneously set up the following three experimental groups, each consisting of pairs of virgin, 14- to 15-segment-long hermaphrodites reared in 10-ml bowls. (1) Conditioned-water treatment: Pairs were set up in clean bowls. Every day the water in the bowl was removed and substituted with conditioned water (29 replicates). (2) Mucous-trail treatment: Pairs were set up in bowls where groups of hermaphrodites had built mucous trails as described before. Water was changed daily with pure water (29 replicates). (3) Control treatment: Pairs were set up in clean bowls where water was exchanged with pure water daily (30 replicates).
All pairs were checked daily for 9 days. We noted the number of newly laid egg-cocoons and the number of eggs per cocoon. Allocation to the female function was measured as the mean number of cocoons and eggs per pair in each of the three experimental groups.
Statistical analysis
Because in experiments the number of cocoons was significantly correlated with the number of eggs (Spearman test, p < .05), only the number of cocoons is reported in Results, unless specified.
Descriptive statistics are reported as means ± standard deviation. When data did not fulfill the assumptions of parametric statistics, they were transformed, and if no suitable transformation could be found, we used non parametric tests. Test probabilities are two tailed (when multiple comparisons were done, probability data were Bonferroni corrected). Data were analyzed with SPSS 7.5.
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RESULTS |
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Group size assessment
The mean number of cocoons per pair was significantly related to the number of potential partners and/or competitors (F1,88 = 47.84, p < .0001, r2 = .35). These results indicate that, in the present experimental conditions, individuals vary their female allocation appropriately to group size (Figure 1).
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Relevance of chemical cues and their species specificity
When paired hermaphrodites received water from conspecifics, they produced significantly fewer cocoons in comparison with those treated with pure water or water conditioned by O. hartmanni individuals (Figure 2) (F2,93= 11.71, p < .001). A posteriori comparisons (Tukey test) showed that highly significant differences exist between the mean number of cocoons produced by hermaphrodites from the conspecific conditioned–water and the control treatment (p < .001) and from the conspecific- and the heterospecific-water treatment (p < .001). In contrast, no significant difference was found between cocoon number per pair from the heterospecific-water and control treatment. These results suggest that a water-borne pheromone was present in the water that we transferred from large groups of mature hermaphrodites to isolated pairs and support the hypothesis that a cue which causes O. diadema worms to change their female allocation is present in the water where large numbers of hermaphrodites were placed. They also indicate that the cue is species specific because it is not present in the water where hermaphrodites of the congeneric species O. hartmanni were placed. Results document that water from O. hartmanni masses does not contain any chemical signal which induces O. diadema individuals to reduce egg production.
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Origin of cues: water-borne versus trail-borne cues
When paired hermaphrodites were subject to the conditioned-water treatment, they produced significantly fewer cocoons per pair than those of the mucous-trail or control treatment (Kruskal-Wallis test: H = 10.72, p = .005) (Figure 3). The conditioned-water treatment caused a significant reduction in the number of eggs produced by hermaphrodites compared to those produced in both the mucous-trail (Mann-Whitney U test, U = 178, p < .0001) and control treatment (Mann-Whitney U test, U = 290, p = .04, n s. after Bonferroni correction). In contrast, egg production did not differ significantly in mucous-trail and control treatment (Mann-Whitney U test, U = 309.5, p = .06).
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These results indicate that the cue which acts as a signal for sex allocation variation is not contained in the mucous trails. Indeed, it is likely that trails facilitate mate encounters (see Premoli and Sella, 1995
). Hermaphrodites from the mucous-trail treatment began laying eggs earlier than those from the other two groups because the number of pairs which laid at least one cocoon within 5 days from the beginning of the experiment was significantly different in the three groups (G test, G = 4.061, df = 1, p < .05) and was the highest in the mucous-trail treatment (Figure 4). Probably, animals that did not have to build mucous trails started to lay eggs earlier than those that had to build mucous trails just because they saved the energy necessary to build such structures.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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O. diadema hermaphrodites adaptively adjust their sex allocation to the number of potential partners and reproductive competitors (Lorenzi et al., in press
). Here we show that, with three different numbers of conspecifics, they regulate their female allocation as a function of those numbers, i.e., by diminishing resources allocated to the female sex as the group size increases.
It is useful to compare our results with recent studies on the mechanistic basis of sex ratio manipulation in wasps, where precise adjustments are observed. Shuker and West (2004) obtained evidence that Nasonia vitripennis wasps precisely adjust the sex ratio of their brood on the basis of the number of eggs laid by other females within a patch. In O. diadema, we have no information on how much group size varies in nature, and this is the crucial variable in the evolution of sex ratio adjustments (West et al., 2000). Nor do we know how many hermaphrodites may fertilize each cocoon. Indeed, the way pseudocopulation occurs in this taxon (Westheide, 1984) makes it unlikely that fertilization is strictly correlated to the number of worms present and probably limits the number of sperm donors which can sire eggs in a cocoon, even though many hermaphrodites may crowd around it.
We designed our experiments to "simulate" large group size in pair-reared worms. Pairs which received water from groups of conspecific worms behaved as if they lived in large groups, decreasing their female allocation with respect to paired hermaphrodites reared in untreated marine water. These data suggest that mature O. diadema hermaphrodites produce species-specific chemicals which are released in the water and act as a cue as to the number of potential reproductive competitors and/or potential partners. When produced simultaneously by many individuals, the water-borne cue triggers a reduction in the number of eggs produced by a receiver. In this paper, paired hermaphrodites treated with conspecific-conditioned water had no more competition for food or nesting sites than pairs reared in pure water, nor did they mate more often. Nevertheless, their female allocation was lower than in control pairs, suggesting that sex allocation variation is part of a decision-making process based on the perception of exogenous cues.
We can exclude that O. diadema worms estimate group size by using the encounter rate as a cue. If this were the case, we would not have observed the variations in female allocation theoretically expected for large group sizes in the pairs with conditioned water. Schärer and Ladurner (2003) hypothesize that, in order to discriminate between different mating group sizes, Macrostomum sp. hermaphrodites have a mechanism to differentiate between previously and newly encountered members of a group. The results we obtained in O. diadema can be explained without resorting to individual recognition. Moreover, Lorenzi and Sella (2000) showed that paired individuals of this species are unable to recognize their own partners after mating encounters.
In our opinion, all the results we obtained are best explained by the hypothesis that hermaphrodites evaluate group size by means of a species-specific pheromone released by mature individuals. We assume that under natural conditions such a pheromone may encourage partner encounters as it signals the presence of mature hermaphrodites. In paired individuals, the same pheromone may favor the intense, high egg-laying rates during monogamous reciprocation (Sella, 1985). If, for example, pheromone production is correlated with egg maturation, it could carry information on the sexual roles of the two partners. Future research is necessary to test this hypothesis which assumes that each O. diadema hermaphrodite has an advantage if it advertises its own presence and state because it can attract partners. At the same time, the perception of multiple rather than single potential partners and/or rivals for the male function will induce a hermaphrodite to become less female biased.
As a general conclusion, O. diadema worms exhibit behaviors which require sophisticated perceptual mechanisms. Indeed, they can perform mate choice and prefer adults rather than adolescents as sexual partners (Sella, 1985) or adults with ripe rather than immature oocytes (Sella and Lorenzi, 2000). Furthermore, as documented in this paper, they can also estimate the number of potential reproductive competitors or potential partners by means of chemical cues, make the appropriate choice, and shift their sex allocation adaptively.
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ACKNOWLEDGEMENTS |
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We wish to thank L. Schärer, S. West, and two anonymous referees for their helpful comments on previous versions of the manuscript and F. Prendergast for linguistic revision. This research was funded by grants from the Ministero dell'Università e Ricerca Scientifica (Cofin 2000) and the University of Turin (ex 60%) to M.C. L. and G.S.
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