flower
Image: Courtesy of Jill S. Miller

Among plants, having sex organs (flowers) that are both male and female at the same time is the norm. A few species, however, do segregate the sexes. As a result, they are only half as reproductively successful as hermaphroditic species. Biologists have thus puzzled over how separate-sex plants evolved. According to a study published today in the journal Science, polyploidy--the state of having more than the normal two sets of chromosomes--may play a pivotal role.

University of Arizona doctoral candidate Jill S. Miller first observed an association between polyploidy and separate-sex plants while studying the evolutionary history of a genus of spiny shrubs known as Lycium (right). All three North American species of Lycium have segregated sexes; all three are polyploid; and all three are genetically self-compatible--meaning in theory a male flower could fertilize female flower on the same plant. Conventional wisdom holds that separate-sex species should arise in self-fertilizing lineages that have no other means for avoiding inbreeding. Yet the closest relatives of these three Lycium are hermaphroditic and unable to mate with themselves.

As it turns out, multiplication of the chromsome sets, a polyploid event, can lead to sudden self-compatibility in a previously self-incompatible plant. Whereas self-incompatible plants have genes that prevent self-fertilization, they do not have the inbreeding avoidance mechanisms that self-compatible plants have. Thus if a self-incompatible plant suddenly became self-compatible, subsequent inbreeding would likely lead to devastating genetic effects. In that situation, nature would favor a mutant plant producing single-sex flowers because it would be unable at the most basic level to self-fertilize. Hence the single-sex mutation could sweep through a population.

Miller and her advisor Larry Venable therefore propose that a polyploid event occurred in a self-incompatible Lycium ancestor, and that the resulting self-compatibility led to the separation of sexes seen in the three North American species. The same event appears to have occurred independently in the South African lineage of Lyceum. In fact, Miller and Venable have evidence for this scenario occurring at least 20 times in other plants. And more cases may well turn up in the future. "People have studied the evolution of separate sexes in plants for a long time and described a lot of different pathways, and nobody's ever made the explicit connection and tried to look for this particular pathway," Miller observes. "The other thing is it looks like it might be relatively common; and if it is relatively common, that makes it sort of amazing that nobody yet has described it."