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Home , Internal fertilization, Mating, Semen, Sexual conflict

When to be Male, When to be : Gender Role Preferences and Mechanisms in

Hermaphrodites, unlike in where each individual is relegated to one gender, are able to perform both female and male roles when it comes to mating. One might suspect that, given hermaphrodites’ abilities to swap roles as needed, there would be less than is often found among sexually dimorphic species, where research has documented how basic differences in male and female strategies for reproductive success can lead to and the of elaborate and bizarre mating habits and sexual conflict (Leonard, 2006). In reality, however, relatively recent studies on hermaphroditic mating practices have revealed that hermaphrodites can exhibit just as intense and varied forms of mating and sexual conflict as species with two genders (e.g. Michiels and Newman, 1998). Why such conflict if hermaphrodites can take on both male and female roles? The answer lies in the fact that while individuals in a hermaphroditic species can take on both genders when mating with one another, one gender role is often preferred. If two individuals would rather mate in the role of the same gender, therefore, a conflict of interests arises, leading to the development of many curious mating systems among hermaphrodites.

This paper intends to explore some of the various mating systems found in species consisting of simultaneous hermaphrodites (that is, hermaphrodites that can perform both gender roles simultaneously). As with sexually dimorphic species, there is significant variability between hermaphroditic species as far as which gender role is preferred when mating. Even more variability is made possible by the fact that hermaphroditic individuals are not locked into one preferred gender role- rather, such preferences may change over time and be based on a variety of factors (Leonard, 2005). First, we will investigate a species in which the male role is preferred and has led to the development of intense sexual conflict. Next, species in which female gender roles are preferred for mating will be explored, along with some specific mating mechanisms. Following this, there will be a shift towards species that change their gender preferences, looking at species which tend to switch back and forth between male and female mating roles based on certain conditions. In all of these cases, the different behaviors exhibited by the species and the reasons for their specific mating preferences will be discussed. Lastly, a theoretical framework accounting for the different mating systems found in hermaphroditic species will be explored, attempting to clarify why different species exhibit different preferences.

Among hermaphrodites, there are many species in which individuals find it advantageous to adopt the male role when mating. A study by Michiels and Newman

(1998) observed the mating tendencies of Pseudoceros bifurcus, a marine that engages in mating behavior which actually physically harms their mates. P. bifurcus partake in a ritual known as “ fencing”, where two individuals, upon engaging in a mating contest, rear up and attempt to stab one another with their . A successful stab allows an individual to inject into the other partner, which fertilizes the losing partner’s in a process known as hypodermic . Consequently, being stabbed relegates an individual to a female role in which they are hit with the double cost of healing their wounds resulting from the stabbing (it pierces their skin), and having to cope with the costs of being fertilized. For these reasons, individuals within this species prefer the significantly less costly over sperm reception. The authors, in arranging and observing specific pairs of P. bifurcus, found that when both individuals reared up as a sign of sexual advance, the two partook in extended parrying contests, trying to stab the other while vehemently avoiding being stabbed themselves.

Furthermore, most inseminations were found to be unilateral, and even in cases where a stabbed individual was able to stab back, the first to inseminate profited from increased injection times. Clearly, in situations such as this where individuals can inseminate unilaterally, male sex role preferences have led to extreme mating behaviors devoid of reciprocity, but this is not always the case.

Though species such as P. bifurcus may find male sex roles advantageous, some species prefer quite the opposite, instead opting for female sex roles when possible. Dall and Wedell (2005) note that in species where occurs and individuals physically copulate up-close together, requiring some degree of cooperation from both individuals (unlike the contest P. bifurcus partakes in), oftentimes the female role is far preferred. The reason for this is that when an individual donates sperm in these cases, that individual will have limited control over how their sperm is used by their partner, and most sperm will be unused for fertilization purposes anyway. When receiving sperm, however, hermaphrodites playing the female role will not only have their eggs fertilized, but also receive additional nutrients in consuming the surplus sperm (Dall and Wedell,

2005). Unlike in P. bifurcus where male-preference can exist because hermaphrodites acting as males can forcefully inseminate others, hermaphrodites who benefit more from a female role in internal fertilization lack the ability to simply force a partner into inseminating them. If every individual adopted a strictly female orientation when mating, therefore, ultimately no sperm would ever be exchanged and the species would cease to survive. Fortunately, species exhibiting these preferences have adopted strategies to combat this issue.

To cope with conflicts of interest when mating, some female-preferring hermaphrodites have developed more reciprocal forms of mating such as sperm trading.

In a pivotal study, Anthes et al. (2005) were successful in definitively proving such tactics in the sea slug Chelidonura hirundinina. Such slugs are part of a special order which have an open fold of skin, referred to as a sperm groove, where flows from the genital aperture to the penis. Usually, when a couple mates, they begin with simultaneous sperm donation, but this is then followed by individuals switching back and forth, each one donating sperm to the other in turn. By disrupting this sperm groove in some, though, experimenters were able to prevent certain individuals from being able to inseminate during mating without affecting their other copulatory behavior. The experimenters had 57 pairs of the slugs in which one individual had its sperm groove cauterized, rendering it useless, and the other individuals had a nearby functionless area of skin cauterized. There were also 51 pairs of slugs in which both individuals just had a nearby area of skin cauterized to serve as controls. The individuals who had the sperm groove cauterized in this case were effectively cheating the system, since they could be inseminated by other and enjoy the advantages of the female sex role without the male cost of having to donate sperm back to their mating partners. Interestingly, the results showed individuals who were mating with a “cheater” gave significantly fewer penis intromissions to their partners than control individuals. Individuals mating with a cheater also donated fewer intromissions than their partners did (though, of course, the partners’ donations were functionally useless since there was no semen). Lastly, individuals mating with a cheater were more likely to desert their partners than control individuals.

This experiment provides strong evidence of a system has developed where cheaters are identified and punished, ensuring the maintenance of these mating habits among internal fertilizers where female mating roles are preferential (Anthes et al., 2005).

While the previous two species discussed maintained a general preference for one sex role or the other, there exist species of hermaphrodites where individuals’ preferences may change on a per-mating situation basis. Facon and colleagues performed two studies on the hermaphroditic snail Physa acuta, detailing the species’ alternation in sex role preferences (Facon et al., 2007; Facon et al., 2008). In one experiment, the authors observed the mating behavior of 240 pairs of snails. One snail from each pair had been set apart in isolation for either a long period (30 days) or a short period (6 days). The authors found that snails in the long isolation condition tended to prefer female mating roles when given access to mates again, whereas those in the short isolation condition preferred male sexual roles (Facon et al. 2007). In a subsequent experiment, Facon et al.

(2008) raised ten families of snails and, after two weeks of sexual isolation, took three snails from each family and placed one each into three boxes of varying size (so there were ten snails per box). In doing this, the experimenters were recreating differences in the population densities. During the first two days after being placed into the boxes, there was a significant effect of density on number of copulations, with more copulations the higher the density of the box. There was no effect of density on frequency of gender alternation, though, and individuals changed gender at a rate higher than chance.

Individuals also did not demonstrate a tendency to stay with the same partner when switching gender roles (Facon et al., 2008). Taken together, these studies suggest a number of things about the nature of mating in P. acuta. First, unlike in Chelidonura hirundinina, gender alternation is not a form of reciprocity for the snails- they do not change gender to appease a partner, and in fact do not tend to mate with the same partner successively more than chance. Why the change then? The authors suggest that snails may be preferring a given sex role based on the amount of sperm left in their own sperm stores (autosperm) and the amount of outsider sperm left in their reproductive tracts (allosperm). If a snail runs out of autosperm, it would clearly have limited success in the male sex role until its stores can be replenished. Likewise if a snail has an excess of allosperm it can continue to use such sperm to fertilize its eggs and would therefore benefit more from a male orientation until its allosperm runs out. Therefore, following a period of isolation snails would have most likely depleted their allosperm stores while building up their own autosperm, making a female-oriented role the most beneficial (Facon et al., 2007; Facon et al., 2008).

Clearly, as the examples above demonstrate, sex role preferences among hermaphrodites are incredibly variable both between species and within species. Given this range of systems and a lack of consistent patterns, researchers have unsurprisingly struggled to find a universal theory which may account for the many hermaphroditic mating systems. Leonard (2005) detailed some of the issues in trying to apply a universal model which could accurately predict and explain hermaphroditic behavior. Originally,

Bateman’s principle was set forth as an effort to explain sexual selection among both hermaphrodites and species with two . Bateman’s principle states that reproductive success is limited in by a female’s ability to acquire enough resources for production, whereas reproductive success in males is limited just by their access to females and eggs. With empirical testing, however, Bateman’s principle was found to be wildly inaccurate as far as predicting both under what circumstances and in what manner hermaphroditic behavior would occur (Leonard, 2005). An additional theory, known as

Gillespie’s principle, proposed that instead hermaphrodites came about as a variance reducing strategy. The theory maintains that when there are two systems of equal average (for example, hermaphroditism as opposed to species with 2 sexes), the system which provides less variance in reproductive success will be preferable and individuals will have higher fitness. As with Bateman’s principle, however, predictions yielded from this theory failed to hold up to empirical data and did not account for a lot of the variation in hermaphroditic mating systems, especially concerning gender role preferences (Leonard 2005).

Only recently has a theory been proposed which may account for the vast amount of hermaphroditic mating behavior. Anthes et al. (2006) proposed a gender ratio hypothesis as a framework for predicting sex role preferences. This hypothesis was based on the idea that sex role preferences are determined by the potential fitness gain of each mating event, meaning a lot of variability is possible both between and within individuals- a tenet which other theories failed to describe. Preferences were, however, predicted to favor male sex roles more frequently than female sex roles. Furthermore, in factoring the overall mating rate of a species into the model, Anthes et al. (2006) were able to map different types of mating mechanisms (for example, unconditional reciprocity compared to unilateral encounters) as a function of both the mating rate and the sex role preference. As a result, this hypothesis is far more comprehensive than others as far as the vast amount of variation it can potentially account for (see Anthes et al., 2006 for exact relationships between mating rate, sex role preferences, and expected mating mechanism). Indeed, unlike other proposed theories, the current one is able to explain the significantly different mating behaviors of P. bifurcus, C. hirundinina, P. acuta, an impressive feat. The hypothesis remains to be tested thoroughly empirically, however, so while an all-encompassing theory remains a ways off there is certainly progress being made.

The unique interactions between individuals from all kinds of hermaphroditic species provide us with a fascinating glimpse into peculiar mating systems. Whether the habits of the male biased P. bifurcus, the cheater-punishing system C. hirundinina utilizes, the gender-preference switching P. acuta, or any one of the many mating systems found in other hermaphroditic species, studying such unique and specific behaviors offers much in our way of understanding not only hermaphrodites, but mating systems of all species in general. Current research has made formidable progress, but there remains much to discover and future possibilities remain ripe.

References

Anthes, N., Putz, A., Michiels, N.K. 2005. Gender trading in a . Current , 15(19), 792-793.

Anthes, N., Putz, A., Michiels, N.K. 2006. Sex role preferences, gender conflict and sperm trading in simultaneous hermaphrodites: a new framework. Behaviour, 72, 1-12.

Dall, S.R.X. & Wedell, N. 2005. Evolutionary conflict: Sperm wars, phantom inseminations. Current Biology, 15(19), 801-803.

Facon, B., Ravigne, V., Sauteur, L., Goudet, J. 2007. Effect of mating history on gender preference the hermaphroditic snail Physa acuta. Animal Behaviour, 74, 1455- 1461.

Facon, B., Ravigne, V., Sauteur, L., Goudet, J. 2008. Gender-role alternation in the simultaneously hermaphroditic freshwater snail Physa acuta: not with the same partner. Behav Ecol Sociobiol, 62, 713-720.

Leonard, J.L. 2005. Bateman’s Principle and Simultaneous Hermaphrodites: A Paradox. Integrative and Comparative Biology, 45, 856-873.

Leonard, J.L. 2006. Sexual selection: lessons from hermaphrodite mating systems. Integrative and Comparative Biology, 46, 349-367.

Michiels, N.K. & Newman, L.J. (1998). Sex and violence in hermaphrodites. Nature, 39, 647.