Evolutionary Pathway To Separate-Sex Plants

Now, two University of Arizona researchers, doctoral candidate Jill Miller and her advisor Larry Venable, have discovered a new and possibly common pathway for the evolution of separate sexes in plants. Their research, reported in this week's issue of Science [Sept. 29 issue], identifies polyploidy, the multiplication of chromosomes into more than the usual two sets, as a crucial precursor to the evolution of many separate-sex plants.

While studying the evolutionary history of spiny shrubs known as "wolfberries," (Lycium, in the potato/tomato family), Miller noticed that all three North American species that had segregated sexes were also "polyploids," with either four or eight sets of chromosomes instead of the usual two sets. Sensing that this association of polyploidy with separate sexes was not a coincidence, Miller began digging deeper into the connection, looking for the possible involvement of self-fertilization, or inbreeding.

Among plants, many cannot mate with themselves because genes for self-incompatibility prevent it. In other plants, self-fertilization is common. Inbreeding may not cause any problems in plants that habitually self-fertilize, because the negative genetic effects of inbreeding, have over time been "purged" from the genome of the plant. But if a self-incompatible plant suddenly becomes capable of self-fertilization, inbreeding could lead to devastating effects, known as "inbreeding depression".

Such a sudden switch from outbreeding to self-compatibility can be caused by a polyploid event, a doubling (or other multiplication) of chromosomes in a normally diploid plant. Polyploidy is known to disrupt self-incompatibility, making it suddenly possible for the new polyploid plant to self-fertilize.. This self-fertilization would then result in inbreeding depression. Under these conditions, an individual plant that produced single-sex flowers would have a great advantage, because it could never self-fertilize, and so it would never suffer from inbreeding depression. Thus, a single-sex mutation could "invade" a population, resulting in a prevalence of individual plants that only made single-sex flowers.

The three polyploid species of Lycium, which all spring from a common ancestor, are all self-compatible, while their nearest relatives are self-incompatible, and have hermaphroditic flowers. Miller and Venable postulate that a polyploid event occurred along the branch of the family tree leading to the three species, and that the consequent breakdown of self-incompatibility led to the evolution of separate sexes.

In all three species of Lycium, some plants are female, producing only female flowers, while others produce flowers that, while hermaphroditic in appearance, really only function as males. This condition, known as gynodioecy, is a stepping-stone on the path to dioecy, the complete separation of the sexes. Among plants whose sexual systems are known, about 72% are hermaphroditic, about 4% dioecious, and about 7% gynodioecious.

Based on previous work by other researchers on the South African species of Lycium, Miller and Venable believe that this scenario may also have occurred independently in that lineage. The South African plants are further along in the process, having evolved completely separate sexes. Furthermore, Miller and Venable have uncovered strong comparative evidence for this same scenario occurring as least 20 times in other plants, and many other possible occurrences may await discovery.

The findings of Miller and Venable are significant because the evolution of separate sexes in plants has long been a topic of controversy and study among plant biologists, but this scenario has not been proposed before. It had been previously thought that the separation of sexes would normally arise in lineages that were already self-compatible, since this is a pre-requisite for self-fertilization. Hence, researchers have been searching for, but having trouble finding, a link between separate sexes and self-compatibility. By showing that a polyploid event can suddenly break down self-incompatibility, Miller and Venable remove the necessity of finding self-compatible ancestors for separate-sex plants, and show that in these cases, the closet relatives of the separate-sex plants *should* be self-incompatible.

"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," notes Miller. "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."

Polyploidy does not always lead to the evolution of separate sexes, because there are other possible strategies for avoiding inbreeding depression. In fact in most cases, the newly self-compatible plants are able to survive the deleterious effects of inbreeding depression, and eventually "purge" the genome of harmful mutations. Another alternative would be for the plant to develop flowers where the male and female parts are not active at the same time, reducing the possibility of self-fertilization. But the results of Miller and Venable's research suggest that the link between polyploidy and inbreeding depression may be the key to a common, and previously unsuspected, pathway to the evolution of separate sexes in plants.