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Presence of Opposite Sex Can Shorten Life Span

29 November 2013 8:00 am
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Let me live, baby. A male fruit fly (left) tantalized by the scent of a female (right) will die prematurely.

Courtesy of Christi Gendron

Let me live, baby. A male fruit fly (left) tantalized by the scent of a female (right) will die prematurely.

In the 1970s pop hit “Paradise by the Dashboard Light,” famed rocker Meat Loaf wails to his tired old lover: “[I]f I gotta spend another minute with you I don't think that I can really survive.” Turns out that interactions with the opposite sex really do control life span, at least if you’re an insect or a worm. Sexually frustrated fruit flies perish prematurely, a study has just found. And another experiment reveals that in nematodes—nearly microscopic roundworms—males kill members of the opposite sex by spurring what resembles premature aging.

An animal’s environment shapes its longevity, sometimes in surprising ways. For example, placing lab animals on a meager diet that replicates food scarcity in the wild extends survival in many species. And, oddly enough, dulling nematodes’ and flies’ sense of smell or taste stretches their life span. An animal’s environment also includes the other members of its species that it interacts with, such as potential mates and rivals. Researchers have identified some impacts of these interactions on life span. For example, because a male fruit fly’s seminal fluid contains toxins, mating can be fatal for females.

Now, Scott Pletcher, a geneticist at the University of Michigan, Ann Arbor, and colleagues have shown that sexually unsatisfied fruit flies give up the ghost faster that usual. The researchers played a dirty trick on some male fruit flies, housing them with other males that had been genetically altered to exude female pheromones, or scent molecules. Normal males woo these she-males but can’t mate with them. Pletcher and colleagues report online today in Science that the sexually thwarted males pined away. Their stored fat dwindled, their ability to endure stress declined, and their life span shrank by more than 10%. The researchers also measured a reduction in female flies’ longevity if they hobnobbed with macho females that released male pheromones.  

Male flies detect the faux females not with their sense of smell, but with their sense of taste, using cells on their forelegs, the researchers found. The team also pinpointed neurons in the male fly brain that were necessary for the truncated life span. These cells produce the protein neuropeptide F, which might enable the animals to respond to rewards, or beneficial stimuli such as mating. “The simplest way to think about it is that the flies are frustrated,” Pletcher says. “The imbalance between mating reward and mating expectation” may trigger physiological responses that spur the animals to waste away, he suggests.

In the other study, Anne Brunet, a geneticist at Stanford University in Palo Alto, California, and colleagues found that in nematodes, the mere trace of one sex also seems to reduce the survival of the other. The nematode species that scientists typically study in the lab has two sexes—males, which constitute less than 1% of the population, and hermaphrodites, which produce sperm and eggs. Previous studies reported that hermaphrodites die sooner in the presence of male nematodes, and researchers suggested that hermaphrodites mate so much in this situation that they suffer injuries and expire.

To test that idea, Brunet and colleagues placed males in culture dishes for 2 days, and then removed them and added hermaphrodites. Despite the absence of males, hermaphrodites still died before their time, the researchers reveal online today in Science. “Males are inducing a premature deterioration of the opposite sex,” Brunet says. This decline resembles premature aging—the worms slow down or become paralyzed, and their muscles and internal organs begin to degenerate. Like flies, male worms exert their life-shortening influence at least partly through pheromones, the researchers found. Mutant hermaphrodites that can’t sense pheromones show a normal life span in the presence of males.

The finding poses an evolutionary puzzle. Hermaphrodites fertilize their own eggs, but males can sire offspring only by mating with hermaphrodites. So why do males kill the mothers of their babies? One possible reason, Brunet says, is competition among males. A male might trigger the demise of his mate to prevent other males from mating with her. However, Patrick Phillips, an evolutionary geneticist at the University of Oregon in Eugene, says he doubts that nematode males are manipulating hermaphrodites, because the hermaphrodites still live long enough to produce a normal number of offspring.

Nevertheless, Phillips says the papers break new ground. “We’ve known for a long time that mating can be harmful,” he says. But these papers show that “you can have the effects without direct physical contact.” Sean Curran, a biogerontologist at the University of Southern California in Los Angeles, predicts the animals’ ability to influence life span “is going to be a hot topic for discussion for quite a while.”

Whether one sex shortens the lives of people or other vertebrates remains uncertain, and finding out will be tricky, Curran cautions: “It’s a far more complicated question in a mammal.” Indeed, in his angst-laden song, Meat Loaf lives on, reduced to merely “praying for the end of time so I can end my time with you.”

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