Worm sex and spiky sperm

February 3, 2011 § Leave a comment

I feel as if I should slap a PG-13 label on this post, at the very least: it’s all about sex and violence, and highly unedifying behavior.  If you don’t want to know about how flatworms have sex, my advice to you is to stop here.  But if you’re willing to endure mild “ew-w-w, gross”-type reactions in the service of an interesting vignette about evolution, read on.

Sexual selection doesn’t end when a male and a female have chosen to mate.  Not every mating results in a fertilization, and this simple fact leads to strong selection on the form and behavior of sperm.  Furthermore, in species where multiple matings are common the female and the male have conflicting priorities: the male always wants his sperm to be successful, while the female may want to make an active choice between two sperm donors.  In flatworms, the situation is complicated yet further by the fact that they’re hermaphrodites, and so the mantra of “do as you would be done by” has special application.  A recent paper (Schärer et al. 2011.  Mating behavior and the evolution of sperm design.  PNAS doi: 10.1073/pnas.1013892108) shows that different species of flatworms have come up with two radically different solutions to the problem of maximizing their own genetic survival at the cost of their partner’s.

The first solution goes by the name of reciprocal mating.  As a hermaphrodite, each worm has two sets of genital organs.  These are arranged such that both partners can simultaneously penetrate the female organ (the antrum) with their male organ (the stylus), which initially seems very fair and balanced.  But immediately after sex is over, the worm turns on itself and starts sucking the sperm out of the antrum, presumably in an attempt to stop the sperm from reaching the egg.  In species that show this kind of behavior, Schärer et al. find that the sperm have evolved to look very much like fish-hooks, with two stiff lateral bristles that (plausibly) make it harder to suck the sperm out once it’s in.

Nasty as this is, the second solution is nastier.  Instead of making any pretence at cooperation, some types of worms simply attempt to puncture their partner’s skin and insert the sperm directly into his/her body.  This is called “hypodermic mating”, and it’s been seen in several hermaphroditic species before.  In a different flatworm species from the ones studied here, the behavior has been called “penis fencing“: pairs of worms rear up with everted penises and try to inseminate each other while avoiding being inseminated themselves.  This leads to wounding, sometimes even making a hole through the body of the worm.  In species that show this behavior, sucking doesn’t happen and the sperm are generally smaller, with no bristles.  This could be because sperm delivered in this way may have to wriggle through the whole body of the other worm in order to find their way to the eggs: small, mobile sperm and lots of them seems like the right strategy here.

Sperm are the most morphologically diverse of all animal cell types, for reasons that we mostly don’t understand.  Are the differences in sperm morphology in this set of flatworm species really the result of differences in mating behavior? Schärer et al. used DNA sequence to make a phylogenetic tree of 16 closely related flatworms of the genus Macrostomum, and mapped onto this tree the characteristics of each species that relate to reproductive behavior.  They found a total of 5 species with the constellation of characteristics they call “hypodermic mating”: physical characteristics include short stylets with needle-like ends, small, mobile sperm, and a thinner female antrum (which is here used only for egg-laying, not for copulation).  The behavior of these species has not always been measured, but when it has been the hypodermic “attack” style of mating is seen, and no sucking behavior is observed.  Of the 11 other species they looked at, 10 clearly fell into the other pattern: spiky (presumably hard to suck out) sperm, a thickened antrum, reciprocal mating, and sucking (again, the data on behavior isn’t perfect, but it’s strong).  We’ll come back to the remaining 1/11 species in a minute.

From the phylogenetic tree you can see that 4/5 of the hypodermic mating species cluster together, but the 5th, M. hystrix, clusters with the reciprocal mating group and is far from the other hypodermic mating species.  The strong implication is that the reciprocal mating pattern is the ancestral one for this group of species, and the hypodermic mating pattern, complete with all the physical and behavioral traits above, has evolved more than once.  The final species of the 16, M. finlandense, seems to be inbetween the two patterns: its stylet has the hypodermic shape, and the antrum has lost the thickening that you see in reciprocal mating species, but the sperm still have residual spikes.  (The behavior of this species hasn’t yet been studied.) M. finlandense is in yet another part of the phylogenetic tree, surrounded by reciprocal mating species.  Overall, the evidence seems to be strongly in favor of the idea that a whole suite of behaviors and physical characteristics evolve together.  Thus, a shift in mating behavior can dramatically alter the conditions for success imposed upon a sperm.  This changes the features needed to win the competition, providing one explanation for the wild diversity of sperm shapes and sizes.

A note on female control: you would think that the female of a species would evolve some kind of defense against aggressive and damaging behavior like hypodermic mating, and find a way to exert some control over whose sperms end up fertilizing her eggs.  And perhaps she would, if she were a she; but since all the species we’re dealing with here are hermaphroditic, all the individuals are s/hes.  So the evolutionary pressures are not so simple.  It’s desirable to avoid the wounding due to hypodermic mating, but at the same time it’s desirable that you succeed in injecting your sperm into a partner.  For flatworms, it appears, the hypodermic mating pattern is sometimes an advantageous one.

I have never felt so happy not to be a hermaphrodite.

Schärer L, Littlewood DT, Waeschenbach A, Yoshida W, & Vizoso DB (2011). From the Cover: Mating behavior and the evolution of sperm design. Proceedings of the National Academy of Sciences of the United States of America, 108 (4), 1490-5 PMID: 21220334

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