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
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
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
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.”
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
The evoluTion and ReSoluTion of Sexual conflic T in floweRing PlanTS
Project objectives
The majority of flowering plants are hermaphrodites, with both male and female sex functions. Sexual conflict arises where those two different functions require different morphologies, or different behaviours. The aim in the project is to probe the implications of sexual conflict for the phenotypes and genotypes of plants, specifically in the context of transitions between dioecy and hermaphroditism. This is where a population shifts from a dioecious state, where individuals have only one sex function, to hermaphroditism, where they have both.
Project funding
This project is funded by the Swiss National Science Foundation (SNSF).
contact details
Project Coordinator, John Pannell
Pannell Group - Ecology and Evolution of Plant Sexual Systems
University of Lausanne - Switzerland
T: +41 21 692 4170
e: john.pannell[@]unil.ch
w: https://www.unil.ch/dee/en/home/ menuguid/people/group-leaders/prof-johnpannell.html
the Y chromosome. “The ability to produce male flowers is on the other chromosomes - all you need is something to switch those genes on,” says Professor Pannell. “In a dioecious population with separate males and females, the switch is something on the Y chromosome. We don’t know precisely what this switch gene is, but we know roughly where it is on the Y chromosome.”
The switch gene effectively turns on a developmental programme. In Professor Pannell’s experiment, this switch was removed when males and the Y chromosome were removed, so something elsewhere in the genome must have adopted the role of the switch. “Again, we don’t know where that switch gene is, but it’s on one of the nonsex chromosomes, the ones we call the autosomes,” explains Professor Pannell. “We are trying to find those regions in the genome that are implicated in male flower production, and we’ve found several candidate regions. What we don’t know is which of those regions harbours the switch gene, and which are the genes that are being switched on. We do know, however, that different genes are involved, and together they contribute to male flower production in females.”
A number of different genes affect sex expression, yet a single gene may also have more than one effect. Professor Pannell’s group have identified a gene that causes an increase in male flower production, while it also leads to a decrease in female flower production, an example of what is called a pleiotropic effect. “It’s like a trade-off effect, where the same gene alters both male and female sex function,” says Professor Pannell. A
gene that affects sex expression may also have other effects on a plant. “For example, those individuals that express the male sterility mutation have smaller leaves for example, or they produce less nectar. There will thus be other effects of that gene that go beyond sex expression,” explains Professor Pannell.
This program of research has largely centred on the European garden weed Mercurialis annua, yet Professor Pannell is also looking at other plants, such as certain dioecious species of the South African ‘cone bush’ genus Leucadendron, which are often sold by florists in Europe for spectacular floral displays. One interesting finding from this strand of research is that the genes that become sexbiased in their expression also evolve more quickly. “The reason we know that, in this genus, is that we’ve looked at sex expression in a number of related species. Our analysis allowed us to infer what the sex expression was likely to have been in the common ancestors within the genus,” outlines Professor Pannell. By sampling a number of species in the genus, and analysing them comparatively, Professor Pannell’s team has been able to test the idea that the genes that become sex-biased evolve more rapidly because of sexual selection. “But we found that the genes that became sex-biased were already evolving quickly, well before they became sex-biased,” he explains. “We thus need a rather different model to explain the relative speed of evolution of sex-biased genes. It seems, for instance, that the sex-biased genes are simply sampled by the plant from a pool of genes that evolve more quickly – genes whose expression levels perhaps do not matter very much to the plant.”
John Pannell is Professor in Plant Evolution at the University of Lausanne. His main research interests include the evolution of plant gender and sexual dimorphism, as well as the ecology, genetics and evolution of polyploidy.
