UA Botanists Discover New Evolutionary Pathway to Separate-Sex Plants

Sept. 28, 2000

Margrit McIntosh for UA News Services

When it comes to sex, most plants have the best of both worlds: Their sex organs - their flowers - are both male and female. The few species that segregate the sexes have long baffled scientists, because a single-sex plant tends to reproduce less successfully than a plant with flowers of both sexes.

Now, two University of Arizona researchers have discovered a new pathway for the evolution of single-gender plants, which they report in this week's issue of Science [Sept. 29 issue]. Doctoral candidate Jill Miller and her advisor, ecology and evolutionary biology Professor D. Larry Venable, found that single-sex plants of the species they examined have more than the usual two sets of chromosomes.

While studying the evolutionary history of wolfberries, spiny shrubs in the potato/tomato family (Lycium), Miller noticed something unusual. 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. "People have studied the evolution of separate sexes in plants for a long time and described a lot of different pathways, but nobody's ever made the explicit connection and tried to look for this particular pathway," noted Miller.

Despite the presence of both male and female flowers, most plants cannot mate with themselves because self-incompatibility is built into their genes. This arrangement can be seen as a genetic taboo against inbreeding. Although some plants can get away with self-fertilization, in other plants it leads to "inbreeding depression," harmful effects that come from being too inbred.

This is where polyploidy comes in. The presence of more than two sets of chromosomes can disrupt the genetic taboo preventing self-fertilization. A self-incompatible plant thus evolves the ability to reproduce on its own - but not necessarily for its own good. Self-fertilization can still cause inbreeding depression in such plants.

Under these conditions, an individual plant that produced single-sex flowers would have an evolutionary advantage. It could never self-fertilize and so it would never suffer from inbreeding depression. The plant would be fit for long-term survival and the single-sex mutation could become the prevailing lifestyle in certain plant populations.

The three polyploid species of wolfberries studied by Miller and Venable are all single-sex plants, while their nearest relatives are hermaphrodites. The researchers speculate that a polyploid event and consequent breakdown of self-incompatibility led to the evolution of separate sexes in this branch of the family tree. Although the male flowers in the single-sex species appear to share both genders, in actuality they only function as males. But technically these species have one more stepping stone to true gender separation.

Miller and Venable suspect this scenario occurred independently in a South African lineage of the same family, Lycium. The South African plants are further along in the process, having evolved separate-sex flowers that don't even pretend to serve both functions. The researchers also have uncovered strong evidence that the same evolutionary tactic occurred at least 20 times in other plants.

"It looks like it might be relatively common," Miller said. "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 most cases, the newly self-compatible plants are able to survive inbreeding depression and eventually purge their genes of harmful mutations.

An alternate pathway 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.


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