The Flamingo’s Smile (5 page)

1. The female praying mantis (
   Mantis religiosa
   , and several related species) will attack anything smaller than itself that moves. Since males are smaller than females in almost all insects, and since mating requires proximity, male mantises become a premier target. In his classic paper of 1935 (see bibliography), K. Roeder writes: “All accounts agree as to the ferocity of the female, and her tendency to capture and devour the male at any time, whether it be during the courtship or after copulation…. The female may seize and eat the male as she would any other insect.”
         A male therefore approaches mating with the punch line of that terrible old joke about how porcupines do it: very carefully. He creeps up slowly, trying at all costs to keep out of the female’s sight line. If the female turns in his direction, he freezes—for mantises ignore anything that doesn’t move. Roeder writes: “So extreme is this immobility that if a male is in the act of raising a leg when first the female is detected, it will be kept poised in the air for some time, and many curious positions may be observed.” Thus, the male continues to approach like a child playing the street game of “red light”—drawing near while his adversary and potential mate averts her eyes, freezing instantly when she looks around (although the penalty for apprehended motion is death, not a return to the starting line). If the male succeeds in creeping up within springing distance, he makes a fateful leap to the female’s back. If he misses, he’s mantis fodder; if he succeeds, he achieves the Darwinian
   summum bonum
   of potential representation in the next generation. After mating, he falls off as far away as he can and then skedaddles with dispatch.
         So far, the story sounds little like a tale of active male conspiracy in his own demise—the requirement, please remember, for an argument that males are directly selected for sexual cannibalism. Perhaps males are simply trying their darndest to get away, but don’t always make it. The strong argument inheres in that great curiosity mentioned at the outset of this essay: decapitated males perform
   better
   sexually than their intact brothers. Roeder has even discovered the neurological basis for this peculiar situation. Much of insect behavior is “hard wired,” so unlike the flexibility of our own actions (and a primary reason why sociobiological models for ants work so poorly for humans). Copulatory movements are controlled by nerves in the last abdominal ganglion (near the back end). Since it would be inconsistent with normal function (and unseemly as well) for males to perform these copulatory motions continually, they are suppressed by inhibitory centers located in the subesophageal ganglion (near the head). When a female eats her mate’s head, she ingests the subesophageal ganglion, and nothing remains to inhibit copulatory movements. What remains of the male now operates as a nonstop mating machine. It will try to mount anything—pencils, for example—of even vaguely appropriate size or shape. Often it finds the female and succeeds in making of its coming death the Darwinian antithesis of what Socrates called “a state of nothingness.”
   
2. A hungry female black widow spider is also a formidable eating machine, and courting males must exercise great circumspection. On entering a female’s web, the male taps and tweaks some of her silk lines. If the female charges, the male either beats a hasty retreat or sails quickly away on his own gossamer. If the female does not respond, the male approaches slowly and cautiously, finally cutting the female’s web at several strategic points, thereby reducing her routes of escape or attack. The male often throws several lines of silk about the female, called, inevitably I suppose, the “bridal veil.” They are not strong, and the larger female could surely break them, but she generally does not, and copulation, as they like to say in the technical literature, “then ensues.” The male, blessed with paired organs for transferring sperm, inserts one palp, then, if not yet attacked by the female, the other. Hungry females may then gobble up their mates, completing the double-entendre of a consummation devoutly to be wished.
         The argument for direct selection of sexual cannibalism rests upon two intriguing phenomena of courtship. First, the tip of the male’s palp usually breaks off during copulation and remains behind in the female. Males, thus rendered incomplete, may not be able to mate again; if so, they have become Darwinian ciphers, ripe for removal. (An interesting speculation identifies this broken tip as a “mating plug” selected to prevent the entry of any subsequent male’s sperm. Such natural
   post factum
   chastity belts are common, and of diverse construction, in the world of insects and would make a fine subject for a future essay on the same issue of why sexual selection identifies our evolutionary world as Darwinian.) Second, males show far less avidity and caution in scramming after the fact than they did in approaching before. K. Ross and R.L. Smith write (see bibliography): “Males that succeeded in insemination lingered in the vicinity of their mates or wandered leisurely away. This was in marked contrast with the initial cautious approach and escape strategies characteristic of males prior to insemination.”
   
3. Females of the desert scorpion
   Paruroctonus mesaensis
   are extremely rapacious and will eat anything small enough that they can detect. “Any moving object in the proper size range is attacked without apparent discrimination” (G.A. Polis and R.D. Farley, see bibliography). Since males are smaller than females, they become prime targets and are consumed with avidity. This indiscriminate rapacity presents quite a problem for mating, which, as usual, requires some spatial intimacy. Males have therefore evolved an elaborate courtship ritual, in part to suppress the female’s ordinary appetite.
         The male initiates a series of grasping and kneading movements with his chelicerae (minor claws), then grabs the female’s chela (major claw) with his own and performs the celebrated
   promenade à deux
   , a reciprocal and symmetrical “dance,” pretty as anything you’ll see at Arthur Murray’s. These scorpions do not inseminate females directly by inserting a penis, but rather deposit a spermatophore (a packet of sperm) that the female must then place into her body. Thus, the male leads the female in the
   promenade
   until he finds an appropriate spot. He deposits the spermatophore, usually on a stick or twig, then bats or even stings her, disengages, and runs for his life. If good fortune smiles, the female will let him go and pay proper attention to inserting his spermatophore. But, in two cases out of more than twenty, Polis and Farley found the female munching away on her mate while his spermatophore remained on a nearby stick, presumably for later ingestion through a different aperture.
   

What evidence, then, do these cases provide for selection of sexual cannibalism among males? Do males, for the sake of their genetic continuity, actively elicit (or even passively submit to) the care and feeding of their fertilized eggs with their own bodies? I find little persuasive evidence for such a phenomenon in these cases, and I wonder if it exists at all—although the argument would provide an excellent illustration of a curiosity that makes little sense unless the evolutionary world works for reproductive success of individuals, as Darwinism argues.

The scorpion story, despite its citation among best cases, provides no evidence at all. As I read Polis and Farley, I note only that males try their best to escape after copulation and succeed in a great majority of cases (only two failed). Indeed, their mating behavior, both before and after, seems designed to avoid destruction, not to court it. Before, they turn off the female’s aggressive instincts by marching and stroking. After, they hit and run. That a few fail and get eaten reflects the inevitable odds of any dangerous game that must be played.

Black widow spiders and praying mantises offer more to the theory of direct selection for destruction among males. The spiders seem to be as cautious as scorpions before, but quite lackadaisical after, making little if any attempt to escape from the female’s web. In addition, if the mating plug that they leave in the female debars them from any future patrimony, then they have fully served their Darwinian purpose. As for mantises, the better performance of a headless male might indicate that sex and death have been actively conjoined by selection. Yet, in both these cases, other observations render more than a bit ambiguous any evidence for active selection on males.

As a major problem for both mantises and spiders, we have no good evidence about the frequency of sexual cannibalism. If it occurred always or even often and if the male clearly stopped and just let it happen, then I would be satisfied that this reasonable phenomenon exists. But if it occurs rarely and represents a simple failure to escape, rather than an active offering, then it is a byproduct of other phenomena, not a selected trait in itself. I can find no quantitative data on the percentage of eating after mating either in nature or even in the more unsatisfactory and artificial conditions of a laboratory.

For mantises, I find no evidence for the male’s complicity in his demise. Males are cautious beforehand and zealous to escape thereafter. But the female is big and rapacious; she makes no distinction between a smaller mantis and any other moving prey. As for the curious fact of better performance in decapitated males, I simply don’t know. It could be a direct adaptation for combining sex with consumption, but other interpretations fare just as well in our absence of evidence. Hard-wired behavior must be programmed in some way. Perhaps the system of inhibition by a ganglion in the head and activation by one near the tail evolved in an ancestral lineage long before sexual cannibalism ever arose among mantises. Perhaps it was already in place when female mantises evolved their indiscriminate rapacity. It would then be co-opted, not actively selected, for its useful role in sexual cannibalism. After all, the same system works for females too, although their behavior serves no known evolutionary function. Decapitate a female mantis and you also unleash sexual behavior, including egg laying. If one wishes to argue that the system must have been actively evolved because the female tends to eat first just that portion of the male that unleashes sexuality, I reply with a bit of biology at its most basic: heads are in front and females encounter them first as the male approaches.

The black widow story is also shaky. Males may not try to escape after mating, but is this an active adaptation for consumption or an automatic response to the real adaptation—breaking of the sexual organ and deposition of a mating plug in the female (for such an injury might weaken the male and explain his subsequent lassitude)? Also, male black widows are tiny compared with their mates—only 2 percent or so of the female’s weight. Will such a small meal make enough of a difference? Finally, and most importantly, how often does the female partake of this available meal? If she always ate the exhausted male after mating, I would be more persuaded. But some studies indicate that sexual cannibalism may be rare, even though clearly available as an option for females. Curiously, several articles report that males often stay on the female’s web until they die, often for two weeks or more, and that females leave them alone. Ross and Smith, for example, noticed only one case of sexual cannibalism and wrote: “Only one male of those we observed to succeed in inseminating a female was eaten by its mate immediately after mating. However, several were later found dead in their mates’ webs.”

Why then, in this disturbing absence of evidence, does our literature abound with comments on the obvious evolutionary good sense of sexual cannibalism? For example: “Under some conditions selection should favor the consumption of males by their mates. His probability of being cannibalized should be directly proportional to the male’s future expectation of reproduction.” Or, “Successful males would best serve their biological interests by presenting themselves to their mates as a post-nuptial meal.”

In this hiatus between reasonable hope and actual evidence, we come face to face with a common bias of modern Darwinism. Darwinian theory is fundamentally about natural selection. I do not challenge this emphasis, but believe that we have become overzealous about the power and range of selection by trying to attribute every significant form and behavior to its direct action. In this Darwinian game, no prize is sweeter than a successful selectionist interpretation for phenomena that strike our intuition as senseless. How could a male become a blood meal after mating if selection rules our world? Because, in certain situations, he increases his own reproductive success thereby, our devoted selectionist responds.

But another overarching, yet often forgotten, evolutionary principle usually intervenes and prevents any optimal match between organism and immediate environment—the curious, tortuous, constraining pathways of history. Organisms are not putty before a molding environment or billiard balls before the pool cue of natural selection. Their inherited forms and behaviors constrain and push back; they cannot be quickly transformed to new optimality every time the environment alters.

Every adaptive change brings scores of consequences in its wake, some luckily co-opted for later advantage, others not. Some large females evolve indiscriminate rapacity for their own reasons, and some males suffer the consequences despite their own evolutionary race to escape. Designs evolved for one reason (or no reason) have other consequences, some fortuitously useful. Male mantises can become headless wonders; male black widows remain on the female’s web. Both behaviors may be useful, but we have no evidence that either arose by active selection for male sacrifice. Sexual cannibalism with active male complicity should be favored in many groups (for the conditions of limited opportunity after mating and useful fodder are often met), but it has evolved rarely, if ever. Ask why we don’t see it where it should occur; don’t simply marvel about the wisdom of selection in a few possible cases. History often precludes useful opportunity; you cannot always get there from here. Females may not be sufficiently rapacious, or they may be smaller than males, or so limited in behavioral flexibility that they cannot evolve a system to turn off a general inhibition against cannibalism only after mating and only toward a male.