In a new study of desert-dwelling fruit flies, University of Arizona researchers have discovered that differences among populations are driven by an arms race between the sexes.
In a paper in today's issue of the Proceedings of the Natural Academy of Sciences (PNAS), Lacey Knowles and Theresa Markow report evidence that population divergence in two species of Drosophila is propelled by male-female interactions.
The fruit flies in this study, relatives of the well-known Drosophila melanogaster, live on the rotting flesh of dying cacti.
The theory of an arms race between males and females, with each sex evolving adaptations and counter-adaptations, has recently garnered support from theoretical studies.
This study, however, is one of the few to provide evidence for the arms race using a post-mating character that is manipulated by both males and females.
Previous studies have found that substances in the reproductive tract evolve far more rapidly than substances from other parts of the body. This supports the idea that this acceleration in the evolution of sex traits is related more to sexual conflict than to natural selection.
However, previous studies have almost always examined male substances. This study documents the female's role in the conflict.
"There's lots of documentation of rapid divergence in male proteins," Knowles said, "but there's no data (before this study) on female response other than to show a genotypic interaction between males and females." Knowles is a research associate in the department of ecology and
In this group of fruit flies, after mating, a large opaque mass forms in the reproductive tract of the female. The mass subsides over time, but she cannot lay eggs or mate again until it does. Although the existence of the mass had been known since the 1940s, Knowles and Markow realized it could be a key factor in sexual coevolution in these species.
The authors tracked the size and duration of this "insemination reaction mass" in a series of reciprocal crosses. They studied how the mass differed in matings of flies from the same and different populations of the same species, and also in matings between flies from different species.
They found that the mass was nearly always larger and more long-lasting when flies from differing populations were mated, indicating that the populations are diverging from each other.
The fact that such differences were observed between populations of the same species is strong evidence that traits related to the mass are evolving very rapidly. In turn, this lends critical support to the emerging theory that rapid changes in sex traits, arising from sexual conflict, play an important role in the evolution of new species.
"I was really surprised when we had the first images (of an insemination mass from a cross between two populations of D. mojavensis)," said Markow, Regents' professor of ecology and evolutionary biology and director of the UA Center for Insect Science. "There was still a mass at 16 hours. I was absolutely blown away."
Although the exact nature and origin of the mass is still not well understood, it appears to involve a chemical reaction between the male insemination substances and the chemistry of the female reproductive tract.
Delayed egg-laying and re-mating are to the advantage of the male, because they increase his chances of siring the majority of that female's eggs. It is thus to his advantage to evolve substances that make the reaction mass larger and longer-lasting.
Females, on the other hand, may gain an advantage from multiple matings. Thus they appear to be evolving counter-defenses to the male substances, reducing the size and duration of the mass.
Knowles and Markow are continuing to study sexual conflict in desert fruit flies. "We're working on experiments right now to actually quantify the costs associated with the mass," Knowles said.
They also plan to study interactions between the sexes with regard to two alternate male strategies: offense and defense. In offense, sperm from one male actively competes with sperm from another male in the female reproductive tract. In defense, males manipulate female behavior to avoid even interacting with other males.
"This would be a very neat system to look at that," Knowles said. "You can make predictions how (males) would do in sperm competition wars. So maybe (if they produce) a small mass, they don't manipulate female behavior very much, (but) maybe they're very effective at sperm wars." - By Margrit McIntosh
[Contact: L. Lacey Knowles, Therese A. Markow]