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Can’t Fool These Ladies Female Fish See Right Through False Suitors’ Pickupacts

August 25, 2008

By ELIE DOLGIN

In a dark, damp corner of a University of Wisconsin-Madison laboratory, Jenny Boughman dropped a 3-inch, three-spined female fish into a fish tank, and waited.

She sat perfectly still as she watched a male fish swim out slowly from its nest, beneath a cracked flower pot.

At first, the male didn’t notice the female among the strips of floating green, plastic table cloth that Boughman had ripped up to mimic a seaweed-like plant.

Then he spotted her. He zigged left and zagged right — the fish equivalent of strutting his stuff.

And then he stopped. Instead of waggling to impress the female, he made a beeline straight for her and started nipping at her tail.

Why the abrupt change in behavior? According to Boughman, an assistant professor of zoology at UW-Madison, it’s because the male realized the female he was courting was a different species, so he modified his charms to suit her particular fancy.

The males of two closely related fish species, known as three- spine sticklebacks, are clever gentlemen callers, Boughman discovered. They can decipher which species of female they’re pursuing and tailor their mating tactics accordingly.

The females aren’t fooled, though. The male behavioral bravado can’t mask their true species identity, and the females opt to mate only with those of their own kind.

“They basically reject the male no matter what he does, no matter how vigorously he courts, or how much like her own male he might court,” said Boughman, who will publish her findings in an upcoming issue of the journal Evolution.

“The females just reject the other species of male almost 100 percent of the time.”

Clearly, the females are in control. But the research has implications well-beyond fishy feminism.

“We’re really trying to understand how these mating interactions have shaped the formation of new species,” Boughman said.

Three-spine sticklebacks are commonly found throughout the Northern Hemisphere. But the pair of species that fill Boughman’s aquariums are found only in a handful of lakes in western Canada. What sets these species apart is that they’re so young.

As the glaciers of the last ice age retreated 10,000 to 15,000 years ago, seafaring sticklebacks swam inland in two successive waves, each time getting trapped in the lakes left behind by the melting glaciers.

This produced two distinct, but closely related species — a “benthic” bottom feeder and a “limnetic” open water feeder.

“Million-year-old species are a dime a dozen; 15,000-year-old species are not,” Boughman said.

Such a short period of time is not long enough to make the species genetically incompatible. Yet, for the most part, the fish don’t interbreed. The main question that drives Boughman’s research is: Why not?

Inherited or learned?

The reason, it now seems, is that the females act as the reproductive gatekeepers, preventing males of the wrong species from successfully mating against the species grain.

Boughman wondered, however, whether this female fickleness was instinctively coded in the DNA that makes a limnetic fish limnetic and a benthic fish benthic, or if choosiness was a trait learned through social conditioning.

Together with graduate student Genevieve Kozak, Boughman reared juvenile sticklebacks with fish of the opposite species, and then tested their social preferences in adulthood.

Earlier this year, Boughman and Kozak reported in the journal Behavioral Ecology that both species preferred to associate with members of the species they had been raised with.

“They seem to be like, ‘Oh, I look like that. I want to be with that kind of fish,’ ” said Kozak.

When it came to choosing whom to mate with, however, the researchers found a notable species difference.

If raised with benthic fish, female limnetic sticklebacks favored benthic males. The preference didn’t work the other way around. Benthic females chose to mate with benthic males, no matter what.

Boughman thinks this species difference arises because limnetic sticklebacks are inherently a more outgoing and gregarious fish. As such, “the social species is more tuned in to the social environment,” she said.

Thus, the species refrain from interbreeding largely because of social conditioning in the limnetic species, Boughman said. If the reversed preference persists outside of the laboratory, she noted, it could drive the two species to collapse back into one.

In the wild, however, the two species rarely encounter each other. So, the female preferences usually develop to keep the species distinct. But if lake habitats change and the two species start socializing more, “it could work to undermine the isolation between the two species,” Boughman said.

Mating habits

While females generally control which fish they choose to mate with, those choices are not always respected by their mates.

Once a female has picked a partner, she deposits her eggs in the male’s nest for him to inseminate, guard and then rear. Fish are not perfect watchdogs, though.

Based on genetic evidence, researchers have reported clutches of stickleback eggs fathered by multiple males.

But it was unknown whether the paternal inconsistencies stemmed from egg stealing, where one male nabs a stash of half-fertilized eggs and hurries them back to his own nest, or from “sneak spawning,” where males fertilize eggs in other males’ nests, and then leave them for the cuckolded male to raise.

Boughman wanted to see what has happening for herself. Last summer, she and two colleagues spent three months sitting in a big, yellow canoe on Paxton Lake, an isolated body of water on Texada Island in British Columbia.

For 12 to 14 hours a day, Boughman’s small team peered over the side of the boat, meticulously watching the sticklebacks’ mating behaviors.

One day, Boughman spotted two males: one was a radiant azure- blue with a bright, red throat — the epitome of suave in stickleback seduction — and the other was drab and dull, blending in with the background.

At first, the Don Juan fish wooed all the females. But then the other male dashed in, stole the first male’s egg cache, and hustled them back to his own nest. Now with his trophy stash of eggs, all the females started swooning over the second male.

“He completely turned around the mating success by essentially being an egg thief,” Boughman said.

Evidently, males pilfer eggs. But Boughman saw them sneak spawning, too.

Either form of cuckoldry undermines female choice, she said, and works against females’ central role in controlling reproduction in the species. It can also undermine the entire speciation process.

“The female had selected a male to mate with, but in fact the father of her offspring was not the male that she picked.”

Although the thieving and sneaking Boughman saw was between males of the same species, if habitat conditions change, it could just as easily happen between species, she noted.

All her research is pointing to one overall conclusion: the speciation process is much more fragile than scientists had once thought.

The fish need separate ecological niches to keep them from cajoling and interbreeding. When those ecological divisions break down, so does speciation.

Indeed, two years ago Boughman reported in the journal Molecular Ecology that the two species are starting to hybridize routinely in one British Columbia lake, because an invasive crayfish is disrupting the ecological balance that usually keeps the species apart.

In 1999, the British Columbia three-spine sticklebacks were listed as endangered species.

Boughman hopes that by better understanding what maintains speciation, biologists and conservationists will have a better chance of preventing speciation from effectively happening in reverse.

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