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Fruit fly sex chances rely on a real wing man

Brother flies have each other’s back when it comes to hitting on the ladies. But when a strange dude enters the room, all bets are off, and the lady suffers.

That’s what’s suggested by a study published Thursday in the journal Nature that offers a glimpse into the widely varying and often brutal behaviors of males seeking to extend their genetic code into the next generation.

“Because they have to compete so aggressively with each other, sometimes you can have paradoxical situations where there might be behaviors that enable a male to out-compete another male, but that also have negative side effects for the female,” said Oxford University evolutionary biologist Tommaso Pizzari, lead author of the study.

The result can be what’s known as the tragedy of the commons -- selfish competition depletes a resource.

But such is not always the case -- competition can be brutal or benign.

“We observe a huge amount of variation in how nasty males are to females, and this is true across species, but also within species, across populations,” Pizzari said. “In some populations, males can kill females rather quickly, and in other populations males are much more benign. And we’ve been lacking a theoretical framework to make sense of this variation.”

To figure out how cooperation and competition strategies shift, the zoologists turned to the lowly fruit fly, Drosophila melanogaster. They first exposed females to a trio of genetic brothers (replacing them weekly) for her lifespan, while exposing other females to three males unrelated to one another. During that time, the flies did what the birds and bees do.

They found that females who consorted with the Drosophila brothers had a longer reproductive lifespan, which gave them greater lifetime reproductive success than those exposed to the unrelated males. Their reproductive aging slowed, the study found.

Two categories of competition could have produced the effect. We’re all familiar with the first: male competition for a chance to mate. Without it, we would have neither Hollywood romances nor John Donne’s bawdy elegies. But send the kids from the room: There is ample evidence of post-copulation, or sperm, competition.

Some males produce seminal proteins that kill off other sperm, affecting a promiscuous female’s propensity to seek another mate, and, as collateral damage, shortening female lifespans. A number of beetle species have engaged in a phallic arms race, with ever spikier sexual organs that perforate the female’s reproductive tract, presumably to allow seminal fluid to flow into her bloodstream. And the outright orgies of Amazonian frogs drown females, whose eggs are then rescued by the males.

Such obvious signs of post-copulatory competition were not evident to the Oxford researchers. But neither were more subtle ones.

So they took a closer look at randy males. Trios of varying composition were exposed to females for their lifespans. The trios either were all related, included one stranger, or were composed of three strangers.

There were no differences in mating rates among groups, but fighting erupted much more when there were strangers in the mix. And the brothers, whether in trios or duos, lived longer.

Once again, there appeared to be no post-copulatory differences, as measured by the mating duration, interval between coitus sessions, or egg laying rates among females who moved among the groups.

Those results suggested that the reproductive lifespan effects on females might be attributable to the male pre-mating behaviors. One further check, however, threw an evolutionary wrench into the works.

The researchers used the trio of two brothers with one stranger, and examined paternity. Even though the unrelated male didn’t court or mate more frequently, he still sired more offspring – twice as many as either of the related duo, in fact.

“That’s really puzzling,” Pizzari acknowledged. “We don’t fully understand what is happening there. It is possible we haven’t quantified the right behaviors, the more relevant behaviors.”

Among the unknowns is exactly how flies would know if they are related. Research has shown they glean a lot of information about one another from pheromones, so they could be sensing their kinship relative to the group. “They seem to adjust to kin, but there’s no cognition or volition involved in this,” Pizzari said.

Of course, this is tinkering in a lab, where scientists have sacrificed Drosophila by the millions to resolve all manner of biological questions, Pizzari noted.

“We know every hair on their body and we know their entire genome,” he said. “But there’s been very little interest in finding out what these things actually do in the wild. They’re almost being used as organic computers.”

In a small population, which tends to have high kinship, a “genotype that tends to be nice” probably prevails, Pizzari theorized. In larger populations full of strangers, then the selfishly competing genome might prevail.

But the duo-plus-stranger experiment produced combat, even between the brothers who were in the group majority, Pizzari noted.

A closer look at female physiology and behavior, and at bigger populations of flies, could offer clues in further research, Pizzari said. Is the paternity advantage of the stranger among two brothers a way to add genetic diversity? That would help the group avoid a population crash, but imperil the female.

“There’s a fine balancing act that the females are facing in terms of optimizing the genetic diversity of their offspring but at the same time avoiding situations where males, because they’re so genetically unrelated to each other, impose high costs on them,” Pizzari said.

In the meantime, he acknowledged, "the smoking gun remains elusive."

Copyright © 2014, Los Angeles Times
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