Everyone with some sort of knowledge on evolution have heard of sexual conflict, how males and females have different interests during reproduction, and sexual selection, i.e., how one sex can influence the evolution of the other.
Sexual organisms are almost always defined by the presence of two sexes: male and female. The male sex is the one that produces the smaller gamete (sexual cell) and the female sex is the one that produces the larger gamete. The male gamete is usually produced in large quantities, because as it is small, it is cheaper to produce. On the other hand, the female gamete is produced in small quantities, because its large size makes it an expensive gamete.
As one can clearly see, the female puts a lot more resources in the production of a single descendant than a male does. As a result, females are usually very choosy regarding who will have the honor to fertilize her eggs. Males need to prove that they are worth the paternity, and female choice, through generations, increase male features that they judge attractive. A classical example is the peacock.
There are a lot of exceptions, of course, most of them driven by the social environment of the species or due to a unusual natural environment which may increase male investment. But all of this stuff refers to dioeicious species, i.e., species in which male and females are separate organisms. But what happens if you are part of a hermaphroditic species, therefore being male and female at the same time? Do you simply mate with anyone? Is everyone versatile everytime they get laid?
Well, there is a lot of diversity in these organism, but all the principles of sexual conflict are still valid. Even if you are male and female at the same time, you still has the desire to fertilize as many eggs as possible with your cheap sperm while choosing carefully who is worth fertilizing your own eggs. The main problem is that anyone else wants the same.
Imagine that you are a hermaphrodite with a handful of expensive eggs and lots of cheap sperm. You are willing to mate and you go on a hunt. Eventually you find another individual with the same intentions. You look each other in the eyes, get closer and start a conversation. Let’s assume that you didn’t find the other one very attractive to be the father of your children, but you whan to be the father of their children.
“So, what are your preferences?” you ask.
“Right now, I wanna be the male” the other one answers.
“Damn!”, you think. Both of you want the same thing. You guys want to play the same sexual role, so there’s a conflict of interests, or, as it is called, a “gender conflict”. In this case, regarding sexual behavior in biology, the word gender refers to the role you play during sex. Who will be the man in the relationship?
In face of this conflict, this hermaphrodite’s dilemma, you both have to find a solution. There are four possible outcomes:
1. You insist on being the male and your partner agrees to play the female against their will. You win, the other one loses.
2. Your partner insists on being the male and you agree to play the female against your will. The other one wins, you lose.
3. Both of you insist on being the male. Sex doesn’t happen and both of you go home without having got laid.
4. Both of you agree to play both roles. Sex happens and you successully deliver your sperm, but is forced to accept the other guy’s sperm too.
The worst for you is not being able to deliver your sperm, as you wished. So 2 and 3 are the worst outcomes. 1 is the better outcome for you, but how will you convince your partner to be the loser? So, the best solution for everyone is 4. Both are neither fully happy nor fully frustrated.
But is this the end? Not necessarily. The most stable mating behavior in a population is indeed to agree to play both roles, but things can go on after you kiss your mate goodbye. Now you have to deal with post-copulatory selection.
You have had sex, you delivered your sperm, but received sperm in return. A low-quality sperm in your opinion. You won’t let that fertilize your eggs, will you? Of course not! So, as soon as your partner is out of sight, you simply spit the sperm out before it reaches your eggs! He will never know.So you cheated your partner! You agreed to receive their sperm in exchange of your own, but then you discarded it as soon as your partner went away. You rule! Right? But… wait! What if they did the same? What if your sperm was discarded too?
You cannot risk that. That would be worse than not having get laid at the first place, because you would have wasted energy and sperm for nothing! But how can you assure that the sperm remains where it is supposed to be?
One strategy is to include some stiff bristles on your sperm cells so that they stick on the inner wall of the female cavity and cannot be removed. The sperm cells function like thorns or spines that go in easily but are very hard to be pulled back. That’s what some flatworms do.Other species evolved a more aggressive approach. They armed their penises with a sharp point that pierces the partners body, forcing it to take the sperm. The sperm is injected in the partner’s tissues and swims towards the eggs.
Both strategies may look like wonderful solutions for the male, but remember that they are hermaphrodites, so that everything can be used against themselves! And that’s the big hermaphrodite’s dilemma, or the ultimate hermaphrodite’s paradox. They are constantly trying to outrun themselves.
Isn’t evolution amazing?
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References and futher reading:
Anthes, N., Putz, A., & Michiels, N. (2006). Hermaphrodite sex role preferences: the role of partner body size, mating history and female fitness in the sea slug Chelidonura sandrana Behavioral Ecology and Sociobiology, 60 (3), 359-367 DOI: 10.1007/s00265-006-0173-5
Janicke, T., Marie-Orleach, L., De Mulder, K., Berezikov, E., Ladurner, P., Vizoso, D., & Schärer, L. (2013). SEX ALLOCATION ADJUSTMENT TO MATING GROUP SIZE IN A SIMULTANEOUS HERMAPHRODITE Evolution, 67 (11), 3233-3242 DOI: 10.1111/evo.12189
Leonard, J. (1990). The Hermaphrodite’s Dilemma Journal of Theoretical Biology, 147 (3), 361-371 DOI: 10.1016/S0022-5193(05)80493-X
Leonard, J., & Lukowiak, K. (1991). Sex and the simultaneous hermaphrodite: testing models of male-female conflict in a sea slug, Navanax intermis (Opisthobranchia) Animal Behaviour, 41 (2), 255-266 DOI: 10.1016/S0003-3472(05)80477-4
Marie-Orleach, L., Janicke, T., & Schärer, L. (2013). Effects of mating status on copulatory and postcopulatory behaviour in a simultaneous hermaphrodite Animal Behaviour, 85 (2), 453-461 DOI: 10.1016/j.anbehav.2012.12.007
Schärer, L., Joss, G., & Sandner, P. (2004). Mating behaviour of the marine turbellarian Macrostomum sp.: these worms suck Marine Biology, 145 (2) DOI: 10.1007/s00227-004-1314-x
Schärer, L., Littlewood, D., Waeschenbach, A., Yoshida, W., & Vizoso, D. (2011). Mating behavior and the evolution of sperm design Proceedings of the National Academy of Sciences, 108 (4), 1490-1495 DOI: 10.1073/pnas.1013892108
Schärer, L., Janicke, T., & Ramm, S. (2015). Sexual Conflict in Hermaphrodites Cold Spring Harbor Perspectives in Biology, 7 (1) DOI: 10.1101/cshperspect.a017673
Wethington, A., & Dillon, JR, R. (1996). Gender choice and gender conflict in a non-reciprocally mating simultaneous hermaphrodite, the freshwater snail,Physa Animal Behaviour, 51 (5), 1107-1118 DOI: 10.1006/anbe.1996.0112
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