The hottest guy guppies stand out in a crowd

Female guppies love a man that sticks out. Or at least they do in the lab. When scientists study the reproduction of the popular aquarium guppy in the laboratory, they often see something called negative frequency-dependent selection, also known as the rare-male effect. That’s when the males with the rare traits, a colorful tail or wild spots, end up fathering the most offspring. But is this just a laboratory effect? And if it isn’t, what does it mean? In an article published October 30 in Nature, Kimberly Hughes and colleagues delve into the rare-male effect and show that rare patterns make for a hot date in the field as they do in the fishbowl.

Male guppies come in truly wild variety of colors and patterns, an effect of their genes. And that in itself is rare. Evolution likes to keep what works best. The rest falls by the wayside. In theory, this means that the most “fit” variations, say, a color that looks poisonous or one particularly attractive to the ladies, would become the most common. By this logic, the many colors of the guppy should have conformed to a single common pattern long ago.

But they haven’t. Instead, the male guppies continue to show not only bright colors but also a high diversity of colors. What keeps the variety going? The rare-male effect. Female guppies prefer the males that are rare, no matter what their color pattern actually is. This effect has been documented in the laboratory in guppies and in other species like fruit flies.

While you can find a lot of great things in the lab, it does bring into question the reality of the rare-male effect. The lab is not the wild, and the pressures of mating in the lab are very different from the pressures of mating in a faraway stream. If you want to determine whether the rare-male effect is a real one, you need to conduct a field experiment.

So Hughes and colleagues went to Trinidad and found natural populations of guppies. In each isolated pool, they caught all the male guppies and sorted them into groups by color and pattern. When the scientists sorted the males, they sorted based on one particular trait: a colorful tail. They found some males that had highly colorful tails and some that had transparent tails (intermediate tails were excluded).

They then returned the fish to the streams, but with an important difference. They returned them in groups where one phenotype, either a colored or transparent tail, was “rare,” by a ratio of about 3 to 1.

After 16 to 17 days, long enough for all the guppies to get their mating on, they went out and fished for the lady guppies. Hughes and her colleagues kept the fish in the lab until the guppies produced their first two broods of offspring. They took those broods and did a very large pile of paternity testing to see which male guppies fathered the most offspring.

And sticking out of the crowd was a hot commodity. For the first brood of offspring, the males that the scientists made “rare” in specific pools had more than twice as many offspring than the males that were more common. The rare-male effect was alive and well in the field.

The scientists also waited for a second brood of baby guppies. Female guppies can store sperm from several matings and use it to fertilize several groups of eggs. While Hughes and colleagues saw the rare-male effect in the first brood of babies, the second told a different story. The rare-male effect was no longer there.

So when it comes to first choice and first brood, the females go with rare males. When it comes to seconds, the results are a little more sloppy. It makes me (and the scientists) wonder about the second brood. It appears that female guppies generally mate more than once, but do they generally not use the stored sperm? The rare male effect worked well for the first brood of offspring, but how strong is it over time?

And, more importantly, what is its purpose? The authors hypothesize that rare-male preference might help to avoid incest. In small, isolated populations, the most common-looking males have a high chance of being related to the females seeking mates. The rare males might thus be less related and therefore a better evolutionary bet, leading to a preference for rare males. A Nature News and Views article on the paper offers some other options. Perhaps rare males have higher survival rates. Maybe the females avoid mating with males that look like their previous mates. It will be interesting to see what future research reveals on why the rare-male effect exists. But whatever the reason, a male guppy should flaunt his differences. They may help make him a dad.