Common sense portends that when the males of a particular species suddenly become scarce, the females will have a tough time finding mates to fertilize their eggs. But new research, led by a group at University College London, finds that females do not resign themselves to forced virginity. Instead they become promiscuous scavengers, taking advantage of a single male's high capacity for mating. The new study appears in this week's issue of Current Biology.
The team, led by UCL biologists Sylvain Charlat and Gregory Hurst, studied 20 populations of the butterfly Hypolimnas bolina, commonly known as the great eggfly or the blue moon butterfly and found in Southeast Asia and on Pacific islands. The populations had female-to-male ratios ranging from nearly even to groups in which females outnumbered males 40 to one. The latter populations were affected by a parasite called Wolbachia, which kills male embryos before they hatch, but does not affect young females. The bacteria are passed from mother to son and can lead to drastically skewed female-to-male ratios.
"When males get rare—due to male-killing bacteria—one would expect females to mate less often since they encounter less males," Charlat says. "What we hadn't realized is the way females would respond to the reduction of spermatophore size."
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The spermatophore is a package of male sperm that is deposited on the female. The researchers were able to monitor the sizes of the spermatophores and found that its diameter per copulation decreased in males that mated with many partners. The scientists wrongly hypothesized that this decrease in average diameter might result from the males rationing their sperm; it turned out, however, that they were running out of resources to distribute. As a result, the females sought more mates to accumulate enough sperm to fertilize all their eggs.
"In fact, the cycle never equilibrates," Charlat explains. "Female mating rates can only increase up to a certain limit, reached when males cannot mate more. This limit was reached in two populations, where females appear to mate less often than they would like because males are just too rare, and exhausted."
Still, this less than ideal quantity of mating does not lead to population depletion, which Hurst pins on the male's high mating capacity. "It's amazing that the numbers of male butterflies can get so low and yet the population is still sustainable and stable," he says. "You don't need many male butterflies to continue the population successfully. This is partly because the decision to mate is mainly under female control and because males have a high mating capacity."
Charlat says that the male-killing effect on population dynamics, which was first discovered by New Zealand scientist Hubert Simmonds in 1920, allows researchers to study how species deal with a scarcity of males. "Wolbachia bacteria are potential tools in biological control," he notes. "It is important to understand their effects in natural populations before such tools are actually developed."
