Resolving sexual conflict in plants
Hermaphroditism is very common in flowering plants, yet separate sexes have evolved in some plants from hermaphroditic ancestors. Why is it that one species has separate sexes, while its sister species in the phylogeny remains hermaphroditic? What changed in the ecology, or the circumstances of the species? These questions are at the core of Professor John Pannell’s research. The vast majority of flowering plants are hermaphrodites, with the ability to perform both male and female sexual functions. As Professor in Plant Evolution at the University of Lausanne, John Pannell is interested in the strategies that the genes in plants use to ensure their own transmission. “To what extent is a population of hermaphrodites maintained in such a state by natural selection?” he asks. In principle, we need to think about a population of hermaphrodites that is challenged by mutations that bring about ‘maleness’ or ‘femaleness’. “Imagine a mutation that emerges in a population of hermaphrodites such that individuals expressing the mutation are no longer able to produce pollen. One might think that expressing such a mutation would be a disadvantage, because the individuals concerned have lost a key mode of transmitting their genes to the next generation. But precisely that sort of mutation is required for a population to evolve towards separate sexes, in which females are just male-sterile hermaphrodites,” explains Professor Pannell. “The question to address is why and when such a sterility mutation should ever be beneficial?”
Sterility mutations A mutation like this would typically be expected to disappear rapidly from the population, as it closes down one avenue towards reproductive success. However, separate sexes have evolved in some plants from hermaphroditic ancestors, so male or female sterility mutations must have
42
The South African species Leucadendron rubrum is one of the most sexually dimorphic plants known. Shown is a male shoot (left) and a female shoot (right). Females have the onerous burden of maintaining their seeds for several years in their seed ‘cones’. Photo by Mathias Scharmann.
been transmitted to subsequent generations in the past. “There must have been cases in the past where a mutation came along in a hermaphroditic population, leading to the loss of the male function for example, and individuals with that mutation then ended up transmitting more genes than their peers in the population,” outlines Professor Pannell. The other hermaphrodites carry on reproducing as before, but as they
are not reproducing as effectively as this new mutant, the male sterility mutation begins to spread in the population. “The new mutation becomes more and more frequent and you get more and more females in the population. We then have a situation where both females and hermaphrodites coexist,” he continues. A plant that has evolved to be only female may also acquire other characteristics over
EU Research
time that enhance its female function, such as a particular morphology that promotes the production and dispersal of seeds. Sexual conflict arises in hermaphrodites when the male and female functions require different morphologies or behaviours. “It is pretty easy to see this in animals, and it applies to plants in much the same way. In mammals, for example, being female requires a physiology that is able to maintain a pregnancy, while being a successful male may require an ability to compete aggressively with other males to mate with the females. Hermaphrodites may suffer from a conflict between these two sexual functions,” says Professor Pannell. This conflict can reduce the reproductive success of hermaphrodites, which is probably one of the reasons why many species of animals have separate sexes. “In a hermaphroditic population in which there’s a strong conflict between the male and female functions, we might well expect mutations to be successful that suppress one sexual function or the other, allowing specialisation in the remaining sexual function,” explains Professor Pannell. In addition to cases where separate sexes have evolved from hermaphroditism, there are also cases where populations have evolved from dioecy to become hermaphroditic. The main advantage of hermaphroditism is commonly viewed as the ability to self-fertilise, but Professor Pannell says the overall picture is more complex than that. “Many flowering plants have mechanisms to prevent self-fertilisation, yet they are still hermaphrodites,” he explains. “So there must be other explanations for maintaining hermaphroditism.” The maintenance of hermaphroditism cannot be attributed simply to the ability to self-fertilise, a topic that Professor Pannell is exploring in his research. Professor Pannell
www.euresearcher.com
and his colleagues have been conducting an experiment for around a decade in which they changed the mating opportunities available in populations of a flowering plant called Mercurialis annua. “We started off with several populations of males and females, and, in some populations, we removed the males,” he outlines. Normally these population would be expected to go extinct due to the lack of mating opportunities, yet this did not always happen. “We tried this experiment three times, and on the first two occasions the populations did effectively go extinct. But every so often in this species – and also in many other plant species with separate sexes – the sexes are not completely separated,” continues Professor Pannell. “Essentially, some females occasionally produce a male flower, or males occasionally produce a female flower.”
their own progeny, but also the progeny of other females in the population. “Imagine a population of 100 female individual plants, all of which produce 10 ovules in their female flowers. If one female now starts to produce pollen, she will be able to fertilise all of her ten seeds, and so produce ten seeds of her own,” explains Professor Pannell. “However, she will also be able to fertilise the seeds produced by all the other females that are not producing pollen. Ultimately, she may expect to see her genes transmitted through all 1,000 progeny produced by the population, whereas those females not producing pollen will have their genes in only their own 10 progeny.” The genes that allowed that first female to produce pollen will now be in the progeny of all those individuals, and so more will have that same ability in subsequent generations.
Why is it that one species has separate sexes, while its sister species in the phylogeny or its ancestor was hermaphroditic? What changed in the ecology, or the circumstances of the species, to facilitate the shift? Sex inconstancy This is called ‘leakiness’ in sex expression, or sex inconstancy, and researchers have found evidence of it in Mercurialis annua. On the third occasion that they conducted this experiment, some of the females showed a degree of sex inconstancy, which gave those females a big advantage in terms of reproductive success. “The inconstant females could produce their own seeds by self-fertilisation, which pure females elsewhere in the population could not do,” says Professor Pannell. The more important factor however is that the females producing pollen were able to sire not only
“Accordingly, we find that the females in the experimental populations quickly evolved to become hermaphrodites, producing more and more male flowers,” says Professor Pannell. It might be expected that a Y chromosome is required to produce pollen, given that pollen production is the male’s function, yet these females do not have a Y chromosome - it was effectively removed from the population with the at the start of the experiment. “It’s clearly not necessary to have a Y chromosome to produce pollen,” outlines Professor Pannell. The genes required for pollen production are thus clearly not located exclusively on
43