Plants, sex & Darwin | University of Oxford
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Plants, sex & Darwin

Pete Wilton

John Pannell of Oxford's Department of Plant Sciences has been studying the mysteries of plant sexuality using Annual Mercury [Mercurialis annua].

A report of his research is published in Current Biology: I asked him about the reproductive choices made by plants, Darwin's views on hermaphoditism and how shifting sexes impact on conservation...

OxSciBlog: What are the evolutionary advantages for plants of being male/female or being hermaphrodite?
John Pannell: Most plants are hermaphrodites. Common intuition is that hermaphrodites benefit from being able to self-fertilise, thus circumventing the need to find a mating partner. This has obvious advantages for sessile [non-mobile] organisms such as plants. However, the vast majority of hermaphroditic plants do everything they can to avoid self-fertilisation because of the deleterious effects of inbreeding on their progeny.

One solution to the problem of selfing is to become a male or a female. While only about 5 per cent of plant species have fully separate sexes, hermaphroditism has been abandoned a great many times in different families, probably often driven by natural selection to avoid inbreeding.

OSB: How did Darwin think shifts between separate sexes and hermaphroditism (or vice-versa) within plant populations occur?
JP: Darwin wrote three books on plant reproduction, one devoted to the problems of self-fertilisation, one to the exquisite adaptations that hermaphrodites have evolved to avoid selfing, and one about plants that have individuals with different types of flowers, including those that are male or female.

He was puzzled about why hermaphroditism should ever have evolved towards separate sexes but realised that hermaphrodites might benefit by becoming specialists in one sexual function or the other. Because reproduction is expensive, specialisation in the production of seeds, say, would cause plants to divert resources away from pollen production. Darwin then saw the evolution of fully separate sexes as the outcome of incremental adjustments in the relative allocation of resources to one sex from the other.

OSB: Why is the herb Mercurialis annua a good plant to use in a study of these shifts?
JP: Mercurialis annua is a wonderful workhorse for studying shifts in the sexual system of plants, for a number of reasons. First, it displays remarkable within-species variation in its sexual system, with some populations being hermaphrodites and others having fully separate sexes.

Even more interesting is the occurrence of populations with an intermediate sexual system, where pure males mate with hermaphrodites. This is a rare sexual system in plants and animals, but its occurrence in Mercurialis annua allowed use to use males to exert a selection pressure in artificial populations on the allocation by hermaphrodites to sexual reproduction.

Because Mercurialis annua is also an annual plant, selections experiments over several generations within a single research project are feasible.

OSB: What has you research revealed about such shifts?
JP: Our research essentially confirmed the prediction that the presence of males in a population of hermaphrodites would cause selection to favour those that biased their allocation to their female function. Similarly, if you remove males from a population that formerly had them, the hermaphrodites are selected to become more male in their allocation.

The experiments thus not only confirm Darwin’s intuition that the sex expression of hermaphrodites responds to natural selection incrementally, but it also provides an illustration of how transitions between hermaphroditism and fully separate sexes can occur.

OSB: What is the significance of shifting sexual patterns to the long-term survival/conservation of plant species?
JP: The research highlights the fact that natural plant populations are in a dynamic balance between changing environments (in this case, whether males occur in the population or not) and responses to natural selection.

We chose for our experiments plant populations that were known to harbour a lot of genetic variation for pollen production, so the fact that hermaphrodites responded to selection is not so surprising. However, many populations of Mercurialis annua, particularly those in the north of the range, have very little genetic variation, and a study of ours published last year in Science showed that these northern population cannot respond to selection nearly as quickly as those in the south.

So, whereas some populations can respond to selection, others may not. Importantly, it is often the marginal populations of a species that are most threatened by environmental change, yet these are precisely the ones that might be less responsive to natural selection because of depleted genetic variation.

Dr John Pannell is based at Oxford's Department of Plant Sciences.