Sexual Cannibals in Gould's Shadow

i-6a43e64c90773719f021f17c0e885650-mantis1.jpgThis female praying mantis is finishing up the last tasty bits of the male that just mated with her. In the lead article in tomorrow's science section of the New York Times, I talk to scientists who study females of some species that sometimes devour their mates. Sexual cannibalism is not common, but it is revealing. The evolutionary forces that shape the sexes can drive them into some extreme conflicts, even turning one sex into a meal for the other. In some cases, males actually become partners in their own demise--passively or complicitly. A new study indicates that male praying mantises are not so willing. They can tell when females are hungry, and they take extra precautions.

I focus on new research in my article, but the history of sexual cannibalism is just as interesting. Scientists have been debating the nature of sexual cannibalism for over twenty years, and their debates capture one of the biggest struggles over how to study evolution. I could only touch briefly on this history in the article, so let me explain here what I mean...

By the late 1970s, a fierce public divide had emerged between some leading evolutionary biologists. They were divided over how to understand the evolutionary history of adaptations. Some--call them adaptationists if you want--argued that much of what we see in animals and other organisms is the finely-tuned product of natural selection. Others--call them exaptationists--argued that evolution is not so free. It works within lots of constraints and is dominated by unpredictable contingencies. If you want to look to an articulate, prominent advocate of each view, look to Richard Dawkins for the adaptationists, and the late Stephen Jay Gould for the exaptationists. (This conflict even spawned a book called Dawkins vs. Gould.) What gave this debate a special kick was its implications for human nature. Adaptationists saw in psychology a collection of behaviors selected and honed for reproductive success. Exaptationists saw this approach as as nothing but a fancy rationalization for justifying entrenched social injustice.

Stephen Jay Gould took advantage of his monthly columns in Natural History from 1976 to 2001 to champion the exaptationist case. One tactic he frequently chose was to pick out a recent adaptationist paper and pick it to pieces. In 1984 he chose the first adaptationist take on sexual cannibalism. In American Naturalist, scientists looked at how a male might benefit by being eaten. They considered the possibility that he could give extra resources to a female, ensuring that his offspring would survive to hatching.

Gould hammered on the paper, in an essay called "Only His Wings Remained.". He argued that adaptationists were seeing adaptations everywhere, like shapes in clouds. Gould reviewed the evidence for sexual cannibalism and concluded it was just the rare byproduct of reflexive attacks from hungry females.

Most of the papers on sexual cannibalism since then cite Gould's essay, but their conclusions often go directly against him. They develop an adaptationist hypothesis, test it, and in some cases find support for it. One of the first examples of this work was that of Maydianne Andrade of the University of Toronto, who showed that male Australian redback spiders somersault into the fangs of their mates--and father more baby spiders in the process. (I described some of her work in my book Evolution: The Triumph of An Idea.)

For many adaptationists, these results were a vindication against Gould and his allies. In 2000, a leading adaptationist, John Alcock, published a withering attack on Gould. He gave special attention to Andrade's work. What Alcock found most objectionable in Gould's writing was not that Gould disagreed with some particular adaptationist hypothesis. It was the way Gould tried to dismiss any adaptationist hypothesis as unworthy of research.

It is certainly true that the hypothesis that got people thinking about sexual cannibalism in 1984--male as meal--has not found support. But there are other ways in which natural selection may favor sexual cannibalism. In some cases, it may give males enough time to stick sperm plugs in females, preventing other males from fertilzing their eggs. In one species of spider, the male dies in coitus. So cannibalism per se is not an adaptation, but the male's death may well be. That's because when the male spider dies, his sexual organs inflate and get stuck in the female.

The latest wrinkle in the sexual cannibalism debates appears once again in the American Naturalist. Scientists found that males adjust their behavior based on how hungry the females are. (You can read the whole paper for free here.) So in one sense, Gould was right: male mantises are not willing partners in their own death. But the paper is more Dawkins than Gould. The male mantises have some way of telling how hungry the females are, and take lots of precautions--jumping on from further away, taking longer to dismount, and so on. These sound like adaptations to me, not historical quirks. And considering how often females try to eat their mates, it's not surprising that male mantises would evolve this sort of self-preserving behavior. As I mention in the article, SUNY biologist William Brown, who carried out the research, is looking into the possibility that females lure males to their doom, not for sex but for lunch. Gould would not approve, I'd imagine, but that's not stopping Brown--or many other biologists.

If all this does not quench your appetite for sexual cannibalism (ugh), check out the Times podcast, where I'm the first guest. And the story comes with some awesome pictures from Catherine Chalmers of the death of one male mantid.


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Posted by: coturnix | September 5, 2006 12:55 AM

By gosh, you are right.
A google search revealed
Results 1 - 10 of about 63,100 for praying mantid.
Results 1 - 10 of about 1,470,000 for preying mantid.
Results 1 - 10 of about 1,770,000 for preying mantis.
Results 1 - 10 of about 1,620,000 for praying mantis
prey or pray?

Nice essay Carl. I think that, while Gould may have overstated the case hugely, he did biology a service by highlighting the role of constraints and phylogeny in evolution and making sure that people thought about them before leaping of into happy adaptationism. Having just gone to the ISBE (International society for Behavioral Ecology) conference and seen a few talks that were really going too far into the just-so story end of things, I think that his work was necessary to make people at least a little more circumspect.

Sharon: I understood that it's "praying" because the way they hold their fore-legs makes them look as though they're, well, praying. I'm not sure that the "count the Google hits" technique is an authoritative way of checking spelling, although a social relativist might say that it is...

By Rob Knell (not verified) on 04 Sep 2006 #permalink

Some research just come out revealing that redback males will preferentially mate with immature females (piercing their exoskeltons in the process as the female doesn't have a genital opening till her last molt). The reason, apparently, is that in so doing they can mate in a position that *doesn't* put them close to their mate's jaws, and thus lets them escape to mate again. So even a seemingly clear-cut adaptationist mating behavior seems to be more complex.

That's because when the male spider dies, his sexual organs inflate and get stuck in the female.

whoa, wicked. do they inflate before he dies or after? if it's after, how do they do that?

I think one huge detail has been left out though. If the males survived mating, would they be able to mate again?

In some species it could be something similar to ageing. They are past their mating abilities, so it doesn't matter what happens to them and so they don't evolve techniques to survive mating. The reasons sexual cannibalism doesn't work in other species is because males can mate many times after mating, so they have a reason to evolve ways of surviving after mating. ...etc.

The reasons sexual cannibalism doesn't work in other species is because males can mate many times after mating, so they have a reason to evolve ways of surviving after mating. ...etc.

Yes, and males tend to forget they focus on the sole act of "mating" (often with as many females as they can), while females are usually looking out for the interests of the offspring, namely for a commitment (not that *all* females stick around to raise their young, either)... but, the male mantid offers nothing, except fulfilment on an instinct driven inside a brain that's about the size of a butt of a needle, so what has the female possibly got to gain by allowing the male live? There's nothing in instinct there, telling the female "this guy is going to stick around for the long haul", might as well get what she can while the getting is good --dinner is the least he can do.

Headless Males Make Great Lovers by Marty Crump
How can it be? Copulatory movements in mantids are controlled by masses of nerve tissue in the abdomen rather than the brain ...

The photo of the mantids on a stark white background drew me in immediately. I knew it had to be a Catherine Chalmers piece. I have her book, Food Chain, on my shelf. Gorgeous!

David Liittschwager and Susan Middleton use a similar style (albeit with a different focus), photographing rare native Hawaiian animals and plants against monochrome backdrops to stunning effect in their books Archipelago and Remains of a Rainbow.

Well sure, avoiding a hungry predator is adaptive. But the point is, it probably did not evolve in the context of copulation. Same thing with the female's predatory urges. They probably were there beforehand.

The science in your Times article was interesting from the perspective of evolutionary biology and the evidence seemed persuasive that Gould overstated his case. Still, I'm not too happy with the sensationalistic way the Times played it.

And about those photos? Don't these insects have blood? Pretty spotless (though lovely) white seamless background...

Hyper-castrating female insects: New York Times, what's your problem? You're creeping me out. Why?

The fact that sexual cannibalism occurs primarily in predatory arthropods with large, agressive females argues strongly for exaptation. Gould might call it "inherent potential." Of course some of the elaborate evasive manuevers of males, especially in spiders does suggest some selective modification

I think the Gould/Dawkins dichotomy, like most, is false. Most evolutionary features, and certainly many behaviors are shaped by a complex interplay of adaptation and exaptation.

As I recall (my copy of the book is AWOL), Sterelny makes the point that Dawkins's and Gould's points of view are not as discrepant as some make them out to be.

I have always heard that if a Praying Mantis feels threatened by a human it will spit in the eyes, which causes the person to go blind. Is this defense mechanism true of a Praying Mantis?