Resource availability drives mating role selection in a simultaneous hermaphrodite Aplysia californica.
Darwin (1859, 1871) observed that, in a great many organisms, males are the sex more eager to mate and females are the more choosy. Since this discovery, male and female roles have been observed to be in conflict across many different clades over concerns related to mating, offspring, and parental care, among other factors (Chapman et al, 2003; Arnqvist and Rowe, 2005). This conflict poses a unique problem for hermaphrodites, particularly simultaneous hermaphrodites, who may take on either the sperm donor ("male") or sperm recipient ("female") role for any given sexual encounter over the course of their mature lives. Not only do they need to select and obtain a partner, they must also determine who will participate in which role, particularly if one of the roles offers a distinct advantage over the other. When individuals prefer the same role, gender conflict occurs (Wethington and Dillon, 1996).
Conventional thinking may lead to the belief that the role with the higher potential fitness, typically the donor role, is unconditionally preferred in simultaneous hermaphrodites (Charnov, 1979; Greeff and Michiels, 1999; Michiels et al, 2003; Anthes et al., 2006b). This idea is demonstrated perhaps most strikingly in the marine flatworm Pseudoceros liparus Marcus, 1950, which engages in behavior popularized as "penis fencing," during which pairs attempt to donate their sperm to one another via hypodermic insemination while actively avoiding being inseminated themselves (Michiels and Newman, 1998). Opportunistic male strategies have also been observed in sea slug species that are more closely related to Aplysia californica, the model used in this study (Michiels et al., 2003; Anthes et al, 2006a). However, other evidence suggests that the recipient role is preferred, particularly in internal fertilizers such as A. californica (Dall and Wedell, 2005; Leonard, 2005; Anthes et al, 2006b). This preference may be the result of sperm storage and digestion mechanisms found in many simultaneous hermaphrodites (Angeloni et al, 2003). Recipients are afforded greater certainty that their gamete investment will result in viable offspring, whereas donors' invested gametes could go unfertilized or be digested, for example.
No matter which role is believed to be advantageous, there is still the question of how gender conflict is handled. One possible solution is a reciprocal mating strategy. If both partners assume both roles, then they take on the same costs and benefits, alleviating potential conflict (Sella, 1988). However, this strategy is vulnerable to "cheaters," who could assume the less costly role initially, then desert their partner. One way that cheating behavior may be mitigated is through successive mating, in which partners alternate roles multiple times, releasing only a small portion of their gametes in each exchange. Such cooperative "egg trading" behavior has been observed in several serranid fish species as well as in polychaete worms (external fertilizers) (Fischer, 1980; Axelrod and Hamilton, 1981; Sella and Ramella, 1999; Sella and Lorenzi, 2000; Erisman and Allen, 2006; Crowley and Hart, 2007; Hart et al., 2016). In instances where the donor role has greater direct investment, one would expect to see reciprocal "sperm trading" instead, such as appears to be the case in several internally fertilizing gastropods (Leonard and Lukowiak, 1985; Anthes et al., 2005; Jordaens et al., 2005; Koene and Ter Maat, 2005; Facon et al., 2008).
The simultaneous hermaphrodite Aplysia californica J. G. Cooper, 1863 is an opisthobranch mollusc that is commonly employed as a model organism in neurophysiology (Frazier et al., 1967). Aplysia californica are terminally reproductive and also mate unilaterally; that is, there is one donor and one recipient for any given encounter (Carefoot, 1987). Aplysia californica are not thought to habitually engage in reciprocal mating behavior in the lab or in the field (Pennings, 1991; Ludwig and Walsh, 2008).
For this study, two sets of controlled mating trials were designed. In the first, Mating I, all experimental animals were placed on unrestricted ad libitum diets to establish mating role selection when both partners had equal access to resources. In the second, Mating II, ad libitum animals were paired with animals on restricted diets to observe if mating role selection changed when one partner occupied a disadvantaged, resource-deprived position. Theory predicts that fitness gains in the donor role are proportionally greater when investments are minimal, and begin to plateau as more resources are expended. Recipient roles, by contrast, are expected to have a more linear relationship between fitness gains and investment (Vizoso and Scharer, 2007). It has been shown experimentally that resource limitation impairs female (but not male) function in a simultaneously hermaphroditic snail (Janicke and Chapuis, 2016). It is therefore expected that resource-deprived animals will participate in the donor role at a greater frequency than their ad libitum counterparts. Their ad libitum partners may respond in kind by selecting a recipient more frequently; however, they may also insist on a reciprocating strategy, as in the gamete trading hypothesis (Leonard and Lukowiak, 1985; Anthes et al., 2006b), or refuse to mate altogether.
Materials and Methods
The specimens of Aplysia californica used in this study were bred and reared in captivity at the NIH-funded National Resource for Aplysia at the University of Miami. Animals were reared in 16-liter, polycarbonate cages submerged in communal fiberglass troughs that received a continuous flow of chilled (15 [degrees]C) seawater to within 2.5 cm of the top of the cage. Each cage received seawater directly from a faucet, with perforations along the cage bottom to optimize flow. Animals were reared one per cage to prevent unobserved copulations. However, animals were likely aware of one another through chemical signals that may have been present in the communal water supply. Each cage was fitted with a weighted panel of perforated styrene "egg crate" to prevent escape. Lighting was kept on a 14:10-hour light:dark cycle. Water temperature ranged from 14.5-15 [degrees]C, approximating the animal's natural range along the California coast (Wayne and Block, 1992). Seawater [O.sub.2] concentration, pH, and salinity were all held at standard hatchery levels (Idrisi et al., 2006). Cages were checked daily for the presence of clutches, which were removed and weighed using an electronic balance.
Original experimental animals
Twelve A. californica specimens were selected from two unrelated sibling groups and weighed to the nearest 0.1 g, using an electronic balance. Weight differences between animals did not exceed 4 g. All animals weighed < 50 g and were not yet sexually mature (Gerdes and Fieber, 2006). The two sibling groups were ages 265 and 241 days at the start of the experiment, which was designated as Day 1. Due to a lack of growth, one animal was replaced during the second week, and two during the third week.
Animals were fed a diet of red macroalgae Agardhiella subulata, which is optimal for inducing growth in Aplysia californica (Gerdes and Fieber, 2006). All animals began the experiment with ad libitum, unrestricted diets. Algae were weighed by electronic balance before being placed in each cage. After 48 h, any remaining algae was removed from cages and reweighed. Prior to weighing, algae were left to air dry for 45-60 min in an effort to minimize the possible effect of excess water on mass. By subtracting the amount of algae removed from the amount of algae added, it was possible to calculate approximately how much algae was consumed over a 24-h period for each animal. After 3 months of ad libitum feeding, half of the animals were moved to a restricted diet. Restricted diets were tailored to each individual and calculated from food intake data during the ad libitum period in relation to the animal's body weight. Restricted diets were calculated from the equation CmXx(Fi/Bm), where x = 0.5 for the first two weeks of restricted feeding, then x = 0.25 for the remainder of the experiment; Fi = mean food intake for a particular animal over a 30-day period of ad libitum feeding; and Bm = mean body mass for the same animal over the same 30-day period. Restricted diets were updated weekly based on the current mass of each animal, represented by Cm. Ad libitum diets were loosely based on each animal's previous feeding history; no ad libitum animals were observed to be without food at any point in the experiment.
[FIGURE 1 OMITTED]
Mating I trials were conducted to observe mating role selection when all animals were on unrestricted ad libitum diets. Trials began on Day 52 of the experiment, when the sibling groups were 293 and 317 days old. Pairs were unrelated (Fig. 1). The effect of body size on role selection is well documented in simultaneous hermaphrodites (see table 2 in Chaine and Angeloni, 2005; Dillen et al, 2008, 2010; Nakadera et al., 2015); however, the relationship has not been strongly supported in A. californica (Zaferes et al., 1988; Pennings, 1991; Angeloni et al, 2003). Nevertheless, potential mates were selected so that the percent difference in mean body mass between them did not exceed 30%; otherwise, pairs were established by random selection. Potential mates were placed together in mating cages and allowed 1 h to engage in mating behavior. Mating behavior was seen to begin after ~20 min in previous experiments (Ludwig and Walsh, 2008). To prevent sperm depletion and to incentivize further mating, copulations were interrupted 15-30 min after mating was initiated. Aplysia californica are not thought to be sperm-limited by copulation periods lasting less than 1 h (Yusa, 1996; Ludwig and Walsh, 2004, 2008). Penis intromission was used as an indicator of successful mating. Sperm donor "attempts" were also recorded. An attempt was categorized by typical sperm donor behavior, in which the head and anterior portion of the foot lean forward between the recipient's parapodia (Leonard and Lukowiak, 1986); however, penis intromission was not observed after the 15 to 30-minute mating period. We assumed that animals who exhibited "attempts" were selecting the sperm-donor role, but their partners were unwilling or unable to act as recipients. Animals were paired randomly under the described criteria for every trial. Trials were conducted once each day, 6 days per week.
On Day 90, a 30-day recess period was imposed, during which no mating trials were conducted. The objective of the recess was to allow the animals time to fully digest any stored allosperm, and for designated animals to acclimate to the new restricted diet. Aplysia californica has been shown to store sperm for 22 [+ or -] 3.6 days (mean [+ or -] SD) (Ludwig and Walsh, 2004). Animals that are allowed time to completely process any potential stored allosperm can be said to be theoretically "reset," which prevents any overlap of cost/benefit associated with either mating role between mating periods (Ludwig and Walsh, 2004).
Mating II trials were conducted to see how mating role selection is influenced when ad libitum animals were paired with those on restricted diets. After the 30-day mating recess, trials resumed on Day 120 of the experiment, when the sibling groups were 360 and 384 days old. Pairs were selected so that animals were matched with an unrelated potential mate on a different diet: ad libitum animals were paired only with restricted-diet animals, and vice versa (Fig. 1). The Mating II trials included supplementary animals so as to adjust for a lack of suitable potential mates. Otherwise, Mating II trials were conducted as in Mating I.
An increase in standard deviation (SD) of mean mass as the animals aged occurred during the experiment. To mitigate concern that there would be insufficient potential mates in the 30%-difference range to constitute mating pairs, 10 animals were added to the experiment on Day 65 in addition to the original 12. These animals belonged to the same two sibling groups as the original groups, but did not participate in the Mating I trials. They were also allocated evenly to the restricted-diet and ad libitum groups (Fig. 1).
[FIGURE 2 OMITTED]
Relative daily intake values used to compare paired donors and recipients were calculated from a polynomial curve of all available data for each individual, [y(x)/z(x)], where y = the intake on Day x, and z = body mass. Paired t-tests compared intake and mass between the donors and recipients of each copulation in order to test the null hypothesis that donors and recipients were not significantly different.
At the onset of the experiment, animals averaged 43.2 [+ or -] 1.2 g (mean [+ or -] SD). For the first 40 days, both growth and food intake proceeded at a relatively stable rate. Food intake began to plateau at approximately Day 40 (age 281 and 305 days). All animals maintained steady growth through the initial mating trials up until Day 92, when feeding regimens were changed and when sibling groups were 356 and 332 days old (Fig. 2). At this point, the mean difference in growth between experimental animals was not significant (unpaired t-test: t = 0.62, df = 10, P = 0.55). Mean mass of restricted-diet animals achieved a maximum at 948.4 [+ or -] 221.2 g, 102% of pre-diet mass 40 days after restricted diets were implemented. In contrast, animals that remained on ad libitum feeding schedules achieved an average maximum mass of 1742.0 [+ or -] 165.9 g, 188.1% of pre-diet values 49 days after restricted diets were implemented for selected animals. Two animals died, presumably from old age at 382 and 396 days, and both from the ad libitum experimental group, before the conclusion of the experiment on Days 141 and 155.
Twenty-six successful copulations occurred over the 39 days of the Mating I trials. Mating behavior was observed on the first day of the trials and throughout Mating I. All but one of the participating animals acted as both sperm donor and sperm recipient over the course of Mating I. Donor attempts were observed 15 times, for an average of 0.38 attempts per day (Table 1). Animals did not consistently alternate between sperm donor and recipient roles over multiple days. However, one instance of immediate reciprocal mating was observed wherein two animals acted as both donor and recipient simultaneously. Donors had less relative food intake than their recipients in 38% of copulations. Over this period, relative food intake did not have a significant impact on mating role selection (paired t-test: t = 0.6, df =25,P = 0.55; Fig. 3).
Mating I trials observed mating role selection when all animals were on unrestricted, ad libitum, diets; Mating II trials studied the influence on mating role selection when ad libitum animals were paired with animals on restricted diets.
[FIGURE 3 OMITTED]
Fourteen successful copulations occurred over the 30 days of the Mating II trials. Donor attempts were observed 18 times, for an average of 0.60 attempts per day (Table 1). As with Mating I, mating behavior was observed on both the first and last day of the trials. Nine of the original experimental animals successfully copulated at least once during the Mating II trials. The lowest intake for an animal acting as a recipient was 3.14% of body mass per day. There were three instances of acting donors and four instances of attempted donors, with intakes below the 3.14% mark. In Mating II trials, donors had less relative food intake than their respective recipients in 85% of copulations (Fig. 3). Relative food intake had a significant (paired t-test: t = 2.4, df = 13, P = 0.03) impact on mating role selection; animals that were consuming relatively less food per day were more likely to act as sperm donors than recipients.
A chi-squared test comparing mating role selection between family groups was not significant; that is, families did not specialize in a particular role (chi-squared test: [chi square] = 1-6, df = 1, P = 0.21). Body size also was not significantly correlated with mating role selection, at least within the established 30% margin in Mating I (paired t-test: t = 0.79, df = 25, P = 0.44) or Mating II (paired t-test: t = 1.7, df = 13, P = 0.12). Over the course of the experiment, some individuals were paired together multiple times. There were a total of 13 replicated pairs in Mating I and 3 pairs in Mating II.
Eleven of the 12 original experimental animals laid at least one clutch of eggs over the course of the experiment. Each animal laid an average of 4.0 [+ or -] 2.3 clutches. Each clutch had an average mass of 37.9 [+ or -] 29.0 g. Ad libitum animals had greater egg yield than the restricted-diet animals in both frequency and mass (Figs. 4, 5). Animals that were placed on restrictive diets had an average clutch mass of 26.7 [+ or -] 19.5 g compared to those fed ad libitum for the entire experiment, whose average clutch mass was 46.2 [+ or -] 32.1 g. Both groups resembled one another closely in both mass and frequency until diets were implemented for restricted animals on Day 90 (Figs. 4, 5).
[FIGURE 4 OMITTED]
As has been noted in earlier studies (Capo et al, 2002; Fieber et al., 2005; Gerdes and Fieber, 2006), the growth of individual animals also varied considerably under laboratory conditions in our study. Animals on ad libitum feeding regimens had greater standard deviations in weekly growth and achieved overall greater mass than animals on restricted diets. Food intake has significant impact on growth (Kriegstein, 1977; Gerdes and Fieber, 2006). The shallower growth curves of animals on restricted diets show that the restricted diets implemented were severe enough to impose a physiological cost to experimental animals. In addition, growth curves of restricted animals plateaued shortly after diets were implemented, much earlier than their ad libitum counterparts. This is noteworthy because it has been observed that Aplysia californica requires significantly less food once sexual maturity is reached (Gerdes and Fieber, 2006). Thus, for diet to have an effect on mating role selection, it is important to establish that restricted diets are sufficiently severe to impose a cost. Animals who are sufficiently resource-deprived presumably will have a preference for the less costly role.
[FIGURE 5 OMITTED]
Mating behavior was observed on both the first and last days of the Mating I and Mating 11 trials, establishing that experimental animals remained sexually active for the duration of the experiment. Lack of observed reciprocation in Mating 1 further supports the idea that reciprocal mating is not a mechanism for mediating gender conflict in A. californica (Pennings, 1991; Ludwig and Walsh, 2008). Nevertheless, one instance of immediate reciprocal mating was observed in which both partners assumed both roles simultaneously. This observation showed that reciprocal mating is possible in A. californica; however, it is not common in hatchery-reared animals. The Mating I trials established that when all animals are fed ad libitum, relative intake is not a factor that influences mating role selection. Animals will select either role regardless of their intake relative to potential partners (Fig. 3).
However, once ad libitum animals were paired with those on restricted diets in the Mating II trials, significant impacts of food intake on mating role selection were discovered. Animals who had restricted diets were significantly more likely to adopt the sperm donor role than their ad libitum counterparts (Fig. 3). Some researchers have suggested that female roles are less costly in simultaneous hermaphrodites; as "recipients," those who play female are not obligated to expend gametes, and may even receive nutritional benefit from digested sperm (Charnov, 1979; De Visser et al, 1994; Charnov, 1996; Eberhard, 1996; Greeff and Michiels, 1999; Chaine and Angeloni, 2005; Dall and Wedell, 2005). Instead, the results suggest that the sperm donor role is less costly in A. californica, as it is the role preferred by animals who must partition their limited resources (Vizoso and Scharer, 2007; Scharer, 2009; Janicke and Chapuis, 2016).
Observations of donor attempts may show that mating roles are determined by the behavior of the resource-deprived partner. Restricted animals more than doubled their rate of attempted donor behavior between Mating I and Mating II (Table 1) (chi-squared test: [chi square] = 4.1, df= 1, P = 0.04). This increased frequency in the donor role is consistent between attempts and observed copulations. By comparison, ad libitum animals attempted the donor role at the same rate in both Mating I and II (chi-squared test: [chi square] = 0.001, df = 1, P = 0.98), but assumed the recipient role in actual copulations more frequently in Mating II. This finding suggests that ad libitum animals accept both roles and exhibit the recipient role more often, only because it is selected more frequently by their potential mates on restricted diets. However, it is worth noting that the frequency of donor attempts was not significant across experimental groups in Mating I (chi-squared test: [chi square] = 0.74, df= 1, P = 0.39) or Mating II (chi-squared test: [chi square] = 1.26, df = 1, P = 0.26).
Interestingly, the proportion of successful copulations did not change significantly between Mating I and II (two-proportion z-test: z = 1.69, P = 0.09). This suggests a lack of increased gender conflict in Mating II. Animals did not refuse to mate with a resource-deprived partner at a greater frequency than when they were paired with an animal of similar condition.
Taken together, these data suggest that both partners benefit from having the animal with the greater access to resources act as sperm recipient. This strategy ensures maximum offspring, because well-fed animals can lay more eggs and, presumably, are less likely to engage in sperm digestion. In terms of which partner controls this dynamic, two scenarios are possible. It could be that resource-deprived animals refuse to accept a more costly recipient role, as is suggested by the observation of donor attempts. However, it may also be that the ad libitum animals refuse to donate sperm to a low-quality recipient who will not be able to produce as many eggs, and who may even eat the donated sperm. The lack of increased gender conflict suggests that the passive partner accepts both roles, or that both partners are able to maximize fitness benefits by adopting complementary roles.
This study clearly demonstrated that individual mating decisions are determined on a case-by-case basis rather than by obligate reciprocation or gamete-trading. It also provides evidence that some simultaneous hermaphrodites are capable of assessing partner condition based on factors that do not seem readily apparent (food intake). Such capabilities have been suggested for other hermaphrodites (Michiels and Bakovski, 2000; Anthes et al., 2006a; Velando et al., 2008; Dominguez and Velando, 2013); however, the mechanisms themselves remain poorly understood (Anthes, 2010). Aplysia californica is an example of a simultaneous hermaphrodite that favors role flexibility in mating, and is able to change strategies over the course of a mating season as a result of shifting environmental variables and partner condition. These findings are supported by Ludwig and Walsh (2008), who came to a similar conclusion concerning multiple mating.
These findings support the gender ratio hypothesis, which posits that simultaneous hermaphrodites make mating decisions based on potential fitness gains for each distinct mating event. The gender ratio predicts that while the male role is generally preferred, the female role will typically also be accepted (Anthes et al., 2006b). This theory allows for a variety of different strategies dependent on the condition of both partners, rather than obligate dependence on any specific strategy. In the Mating I trials, it could be assumed that when mating occurred, the fitness gain in both roles was net positive and, as a result, there was no strong incentive for animals to select one role over the other. However, in Mating II, restricted-diet animals had decreased fitness in the recipient role as a result of their reduced egg output. It then becomes more profitable for both partners to allow the restricted animal to act as donor.
It should be noted that this study observed only interactions between two unrelated cohorts of animals. Any unaccounted factors that may have existed between these particular groups due to genetic background or other sources were not considered. No attempt was made to precisely measure fertilization or sperm investment. It may be beneficial for future studies to take these factors into account in order to obtain a more complete analysis of costs/benefits of mating role selection.
This work was funded by National Institutes of Health Grant no. P40 OD010952. The authors extend profound and sincere thanks to all the staff of the National Resource for Aplysia. Special thanks to Karen David, Mike Simet, Ben Berger, Dr. William Searcy, Dr. Marjorie Oleksiak, Dr. William Drennan, and Dr. Gary Hitchcock, as well as the two anonymous reviewers without whom this work would not have been possible.
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KYLE T. DAVID (*), PHILLIP TANABE, AND LYNNE A. FIEBER
Rosenstiel School of Marine and Atmospheric Science, University of Miami, 4600 Rickenbacker Causeway, Miami, Florida 33149-1098
Received 12 June 2016; accepted 19 September 2016.
(*) To whom correspondence should be addressed. E-mail: firstname.lastname@example.org
Table 1 Average number of donor attempts observed per day for both diets Ad libitum diet Restricted diet Total Mating I 0.23 0.15 0.38 Mating II 0.23 0.37 0.60
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|Author:||David, Kyle T.; Tanabe, Phillip; Fieber, Lynne A.|
|Publication:||The Biological Bulletin|
|Date:||Dec 1, 2016|
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