New research has proposed a genetic explanation for the evolution of a bizarre method used by male butterflies to ensure the success of their sperm

The-Scientist.com, July 29, 2009, by Jef Akst¬† —¬† The sperm of male butterflies has a strange property. About 90% of it is non-fertile — essentially filler for the females’ sperm storage organs that tricks females into thinking they have all the sperm they need to fertilize their eggs. The males’ ploy reduces the likelihood that their mates will take another suitor, thereby ensuring their own paternity. A study published online today (July 29) in Biology Letters suggests that an intense battle of the sexes drove the evolution of non-fertile sperm.

“This study is an elegant and important advance in the understanding of this fascinating male:female co-evolution,” evolutionary biologist Matthew Gage of University of East Anglia in England, who was not involved in the research, wrote in an email to The Scientist.

Nonfertile sperm — or “kamikaze” sperm, as Gage calls them, because they “protect the male’s fertile sperm from competition” — are less costly to produce than fertile sperm. Previous work has suggested that males evolved them specifically to trigger the stretch receptors in the female sperm storage organs that allow them to monitor the amount of sperm in storage, Gage said. This is to the benefit of the male who deposited it, increasing the likelihood he will father a female’s offspring. But it’s to the detriment of the female, limiting the number of large, nutritious spermatophores she receives as gifts from her mates.

Such a conflict of interest between males and females of a species, an evolutionary predicament known as sexual conflict, often leads to genetic connections between the sexually antagonistic traits — in this case, between non-fertile sperm production and the number of mates a female takes. Such a connection might then facilitate the evolution of one or both of the traits. Previous work showed that males produced varying amounts of non-fertile sperm, and that females’ ability to store it varied as well, but until now, there was no evidence for a genetic tie between these two traits.

By comparing butterfly siblings from 25 different families as well as half siblings that shared a father, evolutionary biologist Nina Wedell of the University of Exeter in England and her colleagues found that males that produced more non-fertile sperm had sisters that mated less frequently. These results showed that the two traits are genetically correlated, “a hallmark of sexual conflict,” Wedell said in an email. Furthermore, “the existence of a genetic correlation between sperm production and storage means that, provided the benefit to one sex is larger than the cost in the other sex, the trait can rapidly be elaborated,” Wedell added. That may explain how non-fertile sperm came to compose such an enormous percentage of the ejaculate.

However, the interpretation of Wedell’s results requires some assumptions about the costs and benefits of non-fertile sperm production and storage that have not yet been confirmed, cautioned evolutionary biologist Darryl Gwynne of the University of Toronto, who was not involved in the work. The nutritious gifts that females receive upon mating is likely to be a high incentive for them to mate many times, but there are often costs associated with mating as well. It is therefore unclear how often females should mate to maximize their fitness.

“This paper addresses a really neat potential conflict situation in these butterflies,” Gwynne said, “[but you] need to show [that] by filling her sperm storage organs with these non-fertile sperm and increasing her refractory period, you’re actually impacting her fitness.” In other words, demonstrating that this is a case of sexual conflict requires showing that females incur a cost by storing non-fertile sperm.

In addition to identifying the fitness consequences for females, Wedell and her colleagues want to investigate the variation in male ejaculates. “These butterflies are born with all their sperm,” Wedell explained. “What we would like to know is, how do they decide how much sperm to deliver at each mating?”


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