Maybe half of my audience here will be familiar with this problem. You're a man, and you're hauling this massive, ummm, package around in your pants everywhere you go. Other men fear you, while the women worship you…yet at the same time, your e-mail is stuffed to bursting with strange people making friendly offers to help you make it even bigger. It's a dilemma; you think you would be even more godlike if only it were larger, but could there possibly be any downside to it? (There is a bit of folk wisdom that inflating it drains all the blood from the brain, but this is clearly false. Men who are stupid when erect are also just as stupid when limp.)

A couple of recent studies in fish and spiders have shown that penis size is a matter of competing tradeoffs, and that these compromises have evolutionary consequences. Guys, trash that e-mail for penis enlargement services—they can make you less nimble in pursuit of the ladies, or worse, can get you killed.

Spiders don't have penises, actually; the analogous structures are modified mouthparts called pedipalps that the male charges up with sperm and inserts into the female's ventral opening to inseminate her. (More details on spider sex can be found in the article Spider Kama Sutra). The palps of male spiders have often evolved into quite intricate structures that are keyed to the details of the female's genital opening.

Many spiders exhibit sexual dimorphism as well, typically with the female much larger than the male. In spiders of the genus Tidarren, this trend is carried to an extreme, with males that may be 1% of the female's size. Here's a photo of one of these little guys clinging to his girlfriend's underside, copulating frantically (there is cause for hurry, since she might decide to eat him). While on the one hand the threat of cannibalism might be a reason to be inconspicuous and unnoticed, on the other the male needs to make species-specific displays in order to get so intimate with his mate, and needs pedipalps that she will recognize. Perhaps I'm anthropomorphizing overmuch, but there may also be personal reasons—who wants to be so tiny that the female doesn't even notice when you're mating?

Male and female T. sisyphoides in copula. The minute male (indicated by the arrow) on the female's ventrum is 1% of the female's mass. (The scale bar represents 1 mm.)

Anyway, Tidarren has huge pedipalps. In the photo A below, they are the two gigantic balloon-like structures protruding to the left. Together, they're about the size of his head, and make up about 10% of his mass!

A male T. sisyphoides before (A) and after (B) removing a pedipalp. Note the pedipalps overlap in the two-pedipalp condition (A), whereas the one pedipalp is carried in a central position after pedipalp removal (B). (The scale bars represent 1 mm.)

In B above, we see a curious thing. Spiders have pairs of pedipalps. Shortly after the adult molt, male T. sisyphoides trap one in a bit of spider silk and twist it off. Voluntarily. A kind of willing hemipenectomy. One has to cringe at the thought, but I suppose I can sympathize—if I had a pair of penises the size of volleyballs and weighing 10 pounds each attached to my cheeks, I might want to get rid of one, too.

The question is, what do the spiders gain from this truncation? Vastly improved athletic performance, it turns out.

The authors measured their peak speed in short sprints, and found that it shot up from 2.7±0.2 cm/s to 3.8±0.3. They also had impressive improvements in endurance. They'd chase spiders with a soft brush until the poor fellows collapsed in exhaustion and would move no more. Spiders with two intact pedipalps would flop down after 17 min 30 s±55 s. Lose one palp, and they could keep running for 28 min 30 s±45 s. Even more severe, spiders with two palps died 53% of the time after collapsing, while the unipalp runners only died 12% of the time.

Note that these spiders have unusually massive intromittent organs, and these kinds of performance enhancements would not be achievable in people—these results have no bearing on Lance Armstrong's situation, nor should anyone fear their track coach showing up with a scalpel.

What about vertebrates, then? In another paper, the authors examined the size of the gonopodia in male Gambusia affinis and G. hubbsi, the familiar mosquitofish. The gonopodium is a modified pelvic fin that is used as an intromittent organ, and is a penis-like structure. Different populations exhibit different sizes of gonopodia, and those size differences are retained in the laboratory, so this is a heritable property. Take a look at these representative specimens; which do you think would be more desirable to the ladies, the hunk in A, or the puny girly-fish in B?

Representative laboratory-reared G. affinis males derived from predator-free (A) and predator (B) populations. Arrows indicate the gonopodia. Note the larger gonopodium in A. (Bar, 5 mm.)

The authors tested whether size makes a difference in a clever way, with fish porn. You can show fish videos of other fish, and they react to the images as they would to the real thing, approaching and trying to interact with them. They showed female fish two videos of a male fish, one unretouched, and the other completely identical except that the gonopodium was digitally enhanced to be 15% larger.

Given a choice, females flirted with the large-gonopodium male 81% more often than the small-gonopodium male. You knew that would be the case, didn't you?

Before you rush to open those penis-enlarger ads, though, that advantage doesn't come for free. They also measured burst-speeds in startle-escape responses, the fast tail-flick dart fishes use to get away from the lunge of predators…and the large-gonopodium fish were significantly slower. That large object hanging off the fish represents a good bit of drag, reducing speed, maneuverability, and endurance, and may also be something to catch the eye of predators.

This study went a step further and looked to see if gonopodium size has consequences in the real world. They sampled populations from lakes and ponds that were either free of piscivorous predators (the open bars in the chart below), or contained beasts that would chow down on Gambusia (the black bars), and measured gonopodium size. Males in predator-free waters had gonopodia that were on average 12% larger than their more harried conspecifics.

Divergence in gonopodium size, controlling for body size, between predator regimes in G. affinis (A) and G. hubbsi (B). Data were pooled across years for both species. Least-squares means ± 1 standard error from ANCOVAs are depicted. Open bars represent predator-free populations, and filled bars represent predator populations.

The lesson is clear. If you live in an environment where you can afford to be slow and lazy, sexual selection can take over: the females will preferentially mate with the fish with the larger gonopodia, driving up the average size over generations. If you have to be nimble and swift to stay alive, natural selection will cull out the males with oversized genitals.

Langerhans RB, Layman CA, DeWitt TJ (2005) Male genital size reflects a tradeoff between attracting mates and avoiding predators in two live-bearing fish species. PNAS 102(21):7618-7623.

Ramos M, Irschick DJ, Christenson TE (2004) Overcoming an evolutionary conflict: Removal of a reproductive organ greatly increases locomotor performance. PNAS 101(14):4883-4887.