— Sexy males sire dowdy daughters and attractive females bear insipid sons in fruit flies, at least.
This perverse pattern of inheritance may be one reason why not all individuals are highly attractive. It may even help explain why many of the showiest sexual displays are found in birds and butterflies, rather than other organisms.
The paradox arises because many of the traits that enhance a male's reproductive success are detrimental to female success, and vice versa. For example, female flies that devote a lot of time to feeding may have more energy to put into egg-laying, whereas males may do better spending more of their time mating instead.
"Whenever you have two different gender roles, traits that make a really successful male aren't going to be the ones that make a really successful female," says Alison Pischedda, an evolutionary biologist now at the University of California at Santa Barbara, US.
She and Adam Chippindale, at Queen's University in Kingston, Canada, decided to test how prevalent such genetic conflicts are. They screened a large population of fruit flies to select the three genotypes that were fittest and least fit for each sex. Then they crossed these selected flies in every possible combination and measured the fitness of their offspring.
Low quality offspring
In every case, they found, the fittest mothers produced fitter daughters but less fit sons, compared to less fit mothers. And the fittest fathers produced less fit daughters. The father's genotype had no effect on the fitness of his sons, because most of the genes affecting mating success are on the X sex chromosome, which males inherit only from their mothers. The net result of these differences is that matings between the fittest males and the fittest females produced the lowest-quality offspring.
If this genetic battle of the sexes is prevalent in nature, it would prevent evolution from zeroing in on the most successful genotypes to the exclusion of all others. "If there's continual selection for high-quality males, why isn't every male high-quality?" asks Pischedda. "This could help to explain that."
The balance of this sexual detente is likely to shift somewhat in organisms such as birds and butterflies, Pischedda suggests. Sex determination in these groups is the reverse of the more familiar case of mammals and fruit flies, in which females carry two X chromosomes and males get an X and a Y.
Instead, females have different sex chromosomes called Z and W while males have two copies of the Z. As a result, sexy males can pass their favourable traits directly to their sons, making it easier for such male-only ornaments and behaviours to evolve, she says.
Pischedda and Chippindale's study is the first to show that both male and female parents' success is detrimental to their opposite-sex offspring. However, their experiments used relatively few parental lines.
Further studies are needed to discover whether this evolutionary paradox is actually widespread, says Sarah Otto, an evolutionary biologist at the University of British Columbia in Vancouver, Canada, who was not involved in the study.
Journal reference: Public Library of Science Biology (DOI: 10.1371/journal.pbio.0040356)