Male swordtail of a closely-related species to those used in the study. (Photo: Loury Cédric)

When it comes to reproduction, most fish are external fertilizers, crop dusting eggs in a cloud of sperm. But swordtails (Xiphophorus) aren’t like most fish. These fish fertilize eggs internally and “give birth” to live young. To help this whole operation, males have evolved external genitalia for transferring sperm—a tool not typical among fish. Naturally, the next question would be—for swordtails at least—is bigger better? After all, they went through all the trouble of evolving penises in the first place. New research on the matter of female swordtail preferences towards their males’ members provides an answer: not necessarily. Yes, size is important, but so is how the males use it—and only when females are healthy enough to be in a discerning position.

To be clear, “it” isn’t really like anything familiar to humans. These organs are made of highly-modified portions of a fin near the anus, folded into a long, somewhat terrifying appliance tipped with hooks and weird plates. It’s called a “gonopodium,” and while not technically the same as the mammalian penis—evolutionarily speaking—it functions identically, depositing sperm in the female’s sexual opening. The gonopodium is basically a fish dick, and its length varies wildly between swordtail species and among males in the same species. This makes for a unique opportunity to examine how female choice in mating may be influencing its size.

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Swordtails—guppy-like fish native to Central America’s waterways—get their common name from the males’ bizarrely long extension on the tail fin. In some swordtail species, the males are all “courters,” using their swordtail and showy movements to convince females to permit mating. However, in other species, some males are courters, while others are “sneakers,” small males that skip the complex foreplay step altogether in what’s known as an “alternative reproductive strategy.” The wooing method is passed on directly from the father fish, meaning that courters always sire courter sons, and vice versa with sneakers.

With all this very heritable variation at play between penis length and flirting style in male swordtails, researchers at the Instituto de Ecología, A.C. in Veracruz, México investigated how female fish navigate a chaotic medley of dicks and flashy performances, judging and choosing their preferred partners. By looking at female responses to varying genitalia length, combined with male mating behavior, the scientists were able to narrow down what was important to lady swordtails, and under what conditions.

Their findings—published today in Proceedings B of the Royal Society—show that how female swordtails peruse their suitors’ penises and pageantry may incorporate a careful evolutionary calculus, taking into account survival and risk in a dangerous habitat.

The research team collected both sexes of two species of swordtail from the wild in Mexico for the study: green swordtails (which only have courting males), and high-backed pygmy swordtails (which have both courting and sneaking males). For each species (and each male wooing strategy), they filmed a male interacting and flirting with a female. The resulting short, looped video clip was then Photoshopped frame by frame, removing the female from the clip entirely, and either shortening or lengthening the male’s gonopodium by 30 percent to represent the full range of swordtail dick size. This way, there were six videos: one for each of the three types of males, with each of those divided into long and short-penised versions. They then exposed females to these video clips—shortened and lengthened genitalia versions side by side—and recorded the females’ responses to gauge which version they preferred. This was mostly based on how quickly they approached a video male, and how long they parked in front of the screen.

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Yes, that’s exactly how it sounds: The scientists essentially shot, edited, and screened fish porn to see what got females of the species all hot and bothered.

In the green swordtails, which only have courter males, females preferred the males with smaller junk. The same went for the pygmy swordtails, for both male types. However, as soon as the researchers considered the relative health of the females tested, the preferences split between courters and sneakers.

Before the experiment, all females had their body densities measured, as higher density reflects a body packed with more fat and protein, and thus greater health and “body condition.” Though their more feeble sisters didn’t care much about courtship style (just penis length), heftier, healthier females had very particular tastes. Overall, they favored courter males with short genitalia, but in contrast they liked their sneaker males well hung. As body condition of the females increased, so did the strength of this preference.

Male and female swordtail fish. (Photo: Wojciech J. Płuciennik)

This division in preferences among more weighty female fish likely has its roots in the common quest of all life on Earth: ensuring survival of yourself, and of your offspring. Healthier females are often older, more experienced, and more equipped to evade threats from predators (usually bigger, meaner fish). This allows them to take a bit more risk, and to use their better condition to funnel benefits to the next generation. Under normal conditions, long-dicked males may actually be dangerous to hang around. This is especially true of courter males, which are already conspicuous as hell, attracting attention from predators—long genitalia may actually cause enough drag in the water to make them less able to dart away from danger. Their girlfriends could easily get eaten by association. So, bigger genitalia may just be a bad idea for the courter lifestyle. But for the low-key sneaker males, bigger penises may provide benefits. Mating for them is quick, dirty, and involves chasing, so a longer penis may make fertilization during the athletic feat more likely.

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Given this landscape of penis-size consequences and how males consistently pass on their courtship style to their sons, it’s possible that healthy, risk-taking females are being choosy for the sake of their own potential future sons. By selecting the best combinations of wooing method and penis size, rather than just taking the safest option, these females may be ensuring their sons also have the best packages for the job.

The study illuminates a complex relationship between social behavior, competition, and the evolution of the reproductive system—something we’ve seen before in spring-loaded duck penises—showing us, yet again, that patterns in biology often have indirect causes in hidden, unexpected places.

Jake Buehler is a Seattle area science writer with an adoration for the Tree of Life’s weird, wild, and unsung—follow him on Twitter or at his blog.