When mother mice compete socially for mates in a promiscuous environment, their sons play hard and die young, University of Utah biologists have found. They added that these offspring attract more females by making more urinary pheromones, but smelling sexier shortens their lives.
"If your sons are particularly sexy, and mate more than they would otherwise, it's helping get your genes more efficiently into the next generation," says biology professor Wayne Potts, senior author of the new study.
"Only recently have we started to understand that environmental conditions experienced by parents can influence the characteristics of their offspring. This study is one of the first to show this kind of 'epigenetic' process working in a way that increases the mating success of sons."
Male mice whose parents freely competed for mates in seminatural "mouse barns" produced 31 percent more major urinary proteins or MUPs - sex attractants called pheromones - than male mice from caged monogamous parents, the biologists report online Nov. 18 in the journal Proceedings of the National Academy of Sciences. Pheromone output increased even though the male offspring never competed socially.
Yet the male mice that produced more pheromone had shorter lifespans in another recent study by Potts and Nelson. Only 48 percent of them lived to the end of the experiment, compared with 80 percent of the male mice whose parents lived monogamously in cages. That's likely because it takes so much energy to produce the sex attractants, which are secreted in urine and from certain glands.
"Production of pheromones is outrageously expensive," Potts says. "A single mouse's investment in pheromone production compares with the investment that 10 male peacocks make in the production of their tails, which also are used to attract females."
Female mice prefer scent marks saturated with pheromones produced in mouse urine and other glands, and they mate more often with males who produce such marks. Previous research found that male mice with promiscuous parents actually produce about one-third more progeny than sons of monogamous parents.
The new study illustrates that a mouse's health, lifespan and ability to attract mates depend not only on their parents' genes, but on epigenetics - how parents' environment modifies their offspring's genes to influence how much protein is produced.
"Pheromones are the language of mice," says the study's first author, former University of Utah doctoral student Adam C. Nelson. "When females mate in a socially competitive environment, they program their sons to have a head start by producing more pheromones."
The findings may help programs to breed endangered species in captivity. A more natural way of confining such animals - in social groups rather than lone pairs of mates - may increase their ability to reproduce when later released into the wild.
What does it mean for people? The impacts of social environments on human pheromone output and other traits haven't been studied. "Researchers just have started to scratch the surface of discovering traits that are influenced by parental experience," Potts says. "It is difficult to predict which and how many traits will be involved."
The study was funded by the National Science Foundation and the National Institutes of Health. Potts and Nelson, who is now a postdoctoral fellow at Harvard University, conducted the study with four University of Utah co-authors: oncology professor Bradley Cairns and former doctoral student Andrew Oler at the Huntsman Cancer Institute, and undergraduates Joseph Cauceglia and Seth Merkley. Other co-authors were Neil Youngson at the University of New South Wales in Sydney, Randy Nelson at Ohio State University and Emma Whitelaw of La Trobe University in Melbourne, Australia.
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