Brothers turn female marmots into 'tom boys'
Female yellow-bellied marmots that have many male litter-mates become "tom boys", according to a study of these big, playful rodents.
Developing males produce testosterone, which circulates in the mother's uterus; this male sex hormone "masculinises" the females.
The phenomenon has been seen in many species, but this study shows its long-term impact on animal behaviour.
The findings are published in the Royal Society journal Biology Letters.
Lead researcher Raquel Monclus explained that the results emerged from a 50-year study of the marmots in the Rocky Mountain Biological Laboratory, Colorado.
"We have data from generations of these animals that the lab has gathered," Dr Monclus told BBC Nature.
She carried out the study while at the University of California, Los Angeles, and is now based at the UAM (Universidad Autonoma de Madrid) in Spain.
End Quote Raquel Monclus Universidad Autonoma de Madrid
All juvenile marmots play - in fact most young animals play - but males play more”
"We more or less know everything from when they're born until they die; exactly who is related to who - it's like a big soap opera," she explained.
The physical effects of testosterone were apparent early in this ongoing study, as it was much more difficult for the researchers to correctly identify the sex of newborn females from litters that were mostly male.
"If you think of the uterus as a sealed bottle," said Dr Monclus, "you have five males in there and they are all producing testosterone. So the developing female is getting that dose of testosterone."
The researchers noticed that as these "more male-like" females grew, they would play fight much more than females that were born with lots of sisters.
"All juvenile marmots play - in fact most young animals play - but males play more," explained Dr Monclus.
"One of the theories to explain this is that it prepares them for later life, when they disperse and have to fight to get a new territory and then have to fight again to get access to the females."
As the tom boy females matured, they were also more likely to leave their home territory; behaviour that would usually be expected of males.
The more testosterone a female had been exposed to in the uterus, the more playful and adventurous she was.
Young, masculinised females, Dr Monclus explained, were also less likely to successfully raise their own litter when they first became pregnant.
"There is a relationship with prenatal testosterone and later reproduction," the scientist said. "[Masculinised females] are less successful in their first reproductions."
As well as demonstrating the effects of hormones on developing animals, Dr Monclus and her colleagues believe that the findings show how much of an impact chemicals that mimic the effects of hormones, which are known as endocrine disrupters, could have on wildlife.
"There are lots of these chemicals in the environment - particularly from paper mills and pesticides - that have similar effects," said Dr Monclus.
Professor John Vandenbergh from North Carolina State University has studied the effects of these endocrine-disrupting chemicals and said he was pleased that this "important paper" was being published.
"The [original] discovery that an adjacent male affects an animal's later reproductive anatomy, physiology and behaviour led me and others to study similar effects due to exposure of pregnant females to chemicals such as bisphenol A (BPA)," he told BBC Nature.
"Such endocrine-disrupting compounds are now under active investigation and - in some cases - have been banned.
"This marmot study further reveals the strong effect of low doses of testosterone during pregnancy on another mammal, and that it occurs naturally in the wild."