by Dave Goulson
Of course life might be rather boring in an asexual world, for there would be no peacocks’ tails to impress, no magnificent antlers with which to battle rivals, no beautiful flowers to attract bees. And, of course, no sex. Perhaps fortunately, animals such as the stick insect are in a small minority; the vast majority of animals and plants prefer to have sex in one form or another. It seems that sex confers advantages, although they are hard to pin down precisely. The consensus is that the benefit derives from the mixing of genes from generation to generation, so that endless possible combinations are produced and no two individuals are exactly the same. This makes it possible for favourable combinations of genes to come together, enabling much faster adaptation. It also makes it harder for parasites and diseases to spread, because their hosts are all slightly different from one another, varying in their susceptibility to each disease. It seems that these barely tangible and much-debated advantages outweigh the cost and bother involved in sexual reproduction.
In most animals, individuals are either male or female (of course one might also question why there are two sexes, not three, or four, or fifty-seven, but let’s not go there just yet). In sexual reproduction each sex produces gametes – sperm from males, and eggs from females – and these must come together to form offspring. In contrast, most plants are hermaphrodites: each plant has both male and female sexual organs. More often than not these are contained within the same flower, and they are usually easy to see. The male parts, the anthers, are usually supported on thin stalks and produce powdery pollen, often bright yellow in colour, although it can be white, orange, purple or scarlet. The female parts are often white, generally involving a long stalk with a sticky tip (the stigma) to trap pollen.
Having both male and female parts in the same flower has an obvious disadvantage: it is all too easy for plants to accidentally mate with themselves, which is rarely a good idea except as a last resort. Plants have evolved many mechanisms to avoid this, the simplest of which is to have flowers that are male and female at different times. If you have geraniums1 in your garden, take a close look at the flowers. The young flowers are male, each with ten stamens producing pollen, which is often a distinctive purple colour. After a day or so the stamens wither and the female part ripens, forming a central pillar to the flower, which unfurls into a beautiful five-pointed star, sticky to trap pollen. The male and female versions of the same flower cannot mate with one another because they are separated in time. In foxgloves the flowers hang from a tall stem, with the oldest (female) flowers at the bottom and the youngest (male) flowers at the top, exploiting the fact that bees have the habit of starting at the bottom and working upwards. An arriving bee deposits any pollen she is carrying from another plant on to the stigmas of the lower female flowers before picking up a fresh pollen load from the upper male flowers, which she then carries off to another plant.
Few plants follow the animal model of having distinct sexes, but this small number includes one of the more common flowers in my field in France, the white campion. Campions are distinctive and hence easily recognised plants with five petals, each with a notch or cleft at the margin that is slightly reminiscent of Kirk Douglas’s chin. The flowers of the male and female plants are readily distinguished. The males produce many stamens and yellow pollen that contrasts with the white petals, while the females produce a cluster of twisted, entwined white stigmas. They make attractive garden plants; in my garden in Dunblane I had both white campion and its relatives red campion and ragged robin, the latter with naturally tattered petals. White and red campions flower from May onwards; the female plants are quickly pollinated and pour their energy into producing chunky capsules filled with large, round seeds, so that by the end of June there are few female flowers. In contrast the male plants continue to flower right through the summer until October, a seemingly futile effort, for there is precious little chance of their pollen successfully fertilising a female. The gardener can use this difference between males and females to advantage; by weeding out all but a few female plants, you can ensure far more flowers for longer.
Campions are pollinated by both moths and bees in the familiar mutualistic relationship, providing nectar to attract and reward their pollinators. However, there is an unusual twist, for some of the moths that pollinate them then lay their eggs upon the flowers, gluing them firmly to the petals. One such moth, appropriately named ‘the campion’, feeds exclusively as a caterpillar upon the developing eggs of the female flowers. The small caterpillars live inside the capsule where they are safe from predators, their presence usually given away only by a tiny hole from which protrudes a cluster of droppings, or frass as it is known to us entomologists. Eventually the caterpillars grow too large to reside entirely inside the capsule and bite a larger hole from which their camouflaged but fat rear end protrudes, their head still munching away on the remaining seeds inside. Sometimes, when moth populations are high, almost all of the campion seeds in my field at Chez Nauche are consumed, so it is fortunate that campions are perennial plants that will get further chances to produce seeds in subsequent years.
For campions there is a second risk to sexual reproduction, aside from the danger of attracting egg-eating moths. Campions suffer from one of the most virulent of sexually transmitted diseases of plants, the campion smut Microbotryum violaceum. Smuts are parasitic fungi that are often spread by pollinators and so, in the case of campions, pollinators pose the double threat of both laying eggs that will hatch into voracious larvae and giving the flower a nasty dose of the clap. Smuts have a complex and fascinating life cycle. When fungal spores are delivered by a moth or other pollinator to a campion flower they germinate, sending out thread-like fungal hyphae, which invade the plant tissues. The fungus spreads through the plant, slowly invading right down into the roots. It produces sporidia – the fungal equivalent of sex cells – which are free-living within the host plant. If the plant is infected by more than one ‘mating type’ of smut, then the sporidia from the two different types can fuse: the fungus version of sex. Since there are many different ‘mating types’, and these sex cells are not differentiated into the equivalent of eggs or sperm, there are effectively dozens of different sexes in fungi.
Whether it is infected with one or many mating types of fungus, the plant is doomed to a life of sexual slavery. It seems that they rarely, if ever, throw off their infection. The fungus hijacks the flowers of the plant to its own ends. In a male plant the fungal hyphae invade the anthers so that, instead of producing yellow pollen, they produce fungal spores. These are dark purple in colour, and burst from the anthers even before the flower bud opens, so that when the petals unfurl they are stained purple. It is an ugly sight – the pristine white petals sullied by blotches of purple, which smear like running mascara with rain or dew. In the first year of infection usually just a few flowers are invaded, but by the following year they are all dark with fungal spores, and the plant has lost any chance of reproducing.
When it finds itself in a female campion, the fungus has a further trick up its sleeve. It subverts the development of the female flowers, preventing development of the ovaries and forcing the plant to produce fake anthers, once again bursting with fungal spores. Once they are infected, male and female plants are rather hard to distinguish, although if you pull the flowers apart, the stunted ovaries of the female flowers are still visible.
In some years a great many of the white campion plants at Chez Nauche are infected with smut, to the extent that it can be quite hard to find any healthy flowers. How the species survives in such abundance is something of a mystery to me, for the majority of the population have been effectively sterilised, and any uninfected plant is likely to be exposed to fungal spores very swiftly. Presumably some individual plants have resistance, and the genetic mixing involved in sexual reproduction helps to keep at least some plants one step ahead of the parasite.
I started this chapter with the question ‘Why do males exist?’ A related and equally good question th
at one might ask, but would probably never think to do so, is ‘Why are there usually roughly equal numbers of males and females?’ This is generally true of most animals, and also of plants such as campions in which the sexes are separate. But why? We might accept that sex is useful in allowing genes to be regularly jumbled up, giving scope for speedier evolutionary change, but why do there have to be so many of us males? In most animals, males invest very little in reproduction – sperm are cheap, and one male could cheerfully inseminate numerous females. In red deer, for example, the dominant males defend a huge group of females during the rut and thereby gain exclusive rights to mate with them. Most males aren’t strong enough to compete and so don’t get to mate at all, living out their sad, frustrated lives on the edge of deer society, consumed with jealousy for the monarch of the glen (okay, I’m getting a little carried away now, but you get the idea). So why are so many males produced? Why not just have enough males to go round, and lots more females to produce and rear offspring? A population could certainly grow more rapidly with this arrangement. In fact in fruit flies, females produce more offspring when there aren’t many males about, simply because the males constantly harass them and force them into mating repeatedly, when the females would rather be doing something more useful. The answer was provided by the evolutionary biologist Ronald A. Fisher as long ago as 1930, based at the time at Rothamsted Experimental Station in Hertfordshire. Fisher was a collaborator of E.B. Ford and one of the founders of modern statistics (something that not everyone would thank him for; he invented tests such as Analysis of Variance and, of course, Fisher’s Exact test, which I recall being forced to compute laboriously by hand during A-level maths classes). He suffered from extremely poor eyesight, something that may well have saved his life, for it meant that he was rejected when he enthusiastically and repeatedly attempted to join the army at the outbreak of the First World War.
Fisher’s explanation was remarkably simple. Suppose males are scarce in a particular population. Newborn males in such a population would have better prospects than newborn females, for they would be likely to have more offspring – there would be lots of mates for them. Therefore any parents with genetic tendencies to produce sons would be at an advantage, and their genes would spread. Males would become more common, but as the ratio of males to females approached 1:1, their advantage would disappear, and the genes favouring male production would cease to spread. Exactly the same argument in reverse could be used when starting with a male-biased population, in which the production of daughters would be favoured.
This argument is now known as ‘Fisher’s principle’, and campions provide a rare and interesting exception. In white campions, females are generally more common than males. According to Fisher’s argument, these females should have lower reproductive success than the few lucky males, who benefit from being able to pollinate the many females. Hence natural selection ought to favour individuals to produce more male offspring. Why doesn’t this happen? The answer is complicated, but sufficiently fascinating to be worth explaining. So far as it is understood, the odd sex ratio in campions seems to be the result of a battle that rages between different genes within the plants. Oxford biologist and prominent atheist Richard Dawkins has championed the view that the genes within our body operate on an ‘every gene for himself’ basis. On the whole it is generally in the interests of genes to collaborate, for their chances of propagation into the next generation depend on their host body thriving and reproducing. Sometimes, however, individual ‘selfish’ genes attempt to cheat on this alliance, ensuring their own propagation at the expense of their collaborators.
Most of the genes within the cells of organisms such as humans or campions are packed into chromosomes within the nucleus. A few live outside the nucleus in the cell cytoplasm; there are genes in our mitochondria and in the chloroplasts of plants left over from an ancient time when these cell structures were actually free-living organisms in their own right. These genes are passed down through the maternal line (in eggs, but not in sperm or pollen), so if they find themselves in a male they have reached a dead-end. To reduce the chances of this happening, some cytoplasmic genes distort the ratio of offspring produced by their host, killing male offspring so that more female offspring can be produced. This is bad news for the rest of the genome, for it will find itself within females in a population in which males are scarce and hence have by far the higher reproductive success. It is particularly bad news for genes on the Y chromosome, for they are found only in males and so bear the brunt of this genetic revolt (note that both campions and humans share a system in which females have two X chromosomes and males an X and a Y).
Genes on the Y chromosome don’t take this lying down; the attack of the cytoplasmic genes selects for genes on the Y chromosome that can inactivate the male-killing cytoplasmic genes – so-called ‘restorer genes’. In turn the cytoplasmic genes evolve to evade the blocking action. This battle is ongoing, and so the relative abundance of male and female campions in any particular population is a reflection of the state of the endless war; if the cytoplasmic genes currently have the edge, the females are disproportionately numerous, whereas if the Y-linked genes have successfully knocked them out and gained the upper hand, the ratio is 1:1.
You may well be feeling that this is quite enough genetics for one day, but there is more, for white campions do not operate in genetic isolation; they hybridise with their cousin the red campion, and this has intriguing consequences for the genetic war within. In the UK white campions are more common in the drier, sunnier and more arable east of the country, often occurring in field margins and fallow ground, while red campions are more common in the wetter west; they abound in the banked hedgerows and road verges of Devon and Cornwall. Red campions seem to be more shade-tolerant and damp-loving, often growing in woodland glades and edges, while white campions are usually found out in the open. In some areas, including Hampshire where I used to live, both species are common and frequently occur within close proximity to one another, and in such places pink-flowered hybrids are common. During my field work on bumblebees, travelling around south-central England, I noticed many clusters of pink-flowered campions, but also no shortage of both white and red parents. Ever the scientific dabbler, this struck me as interesting and worthy of study. If the two species can interbreed so easily, what keeps them distinct? Why don’t they just blend together as a mass of pink-flowered campions? Moths and bees do not stick to woods or to meadows, but readily move between the two, so red and white campion females must often receive pollen from males of the other species. Clearly this resulted in offspring: the pink-flowered hybrids. Unless these hybrids were in some way less fit than their parents, and thus were selected out of the population, it was hard to understand how the two parent species maintained their integrity. It was possible that part of the answer might lie in the interaction between the cytoplasmic genes that favour female production and the Y-chromosome restorer genes, for in hybrids these will become separated; Y-linked restorers from one species are unlikely to be effective against cytoplasmic genes from a different species, so we might expect hybrid populations to be heavily female-biased. If there were no males, this could lead to hybrid populations crashing.
I decided to do some experiments. The first step was to check whether the pink hybrids were fully viable and healthy. Some species can interbreed, producing hybrid offspring (lions and tigers, for example), but the hybrids are sterile and so the two species cannot merge together. I crossed red and white campions in the glasshouses at Southampton University, keeping the males and females in separate sections of the glasshouses and pollinating them by hand using a paintbrush. I reared the pink-flowered offspring, which grew vigorously, and the following year I crossed the hybrids with one another and with both parent species. Once again all the offspring were healthy, and I soon ended up with a lovely array of flowers in all shades from white to red. If anything, the hybrids were larger and healthier than their pure-blood parents, which
left unanswered the question of how the parent species remain distinct. Although there were more females than males in the hybrid offspring, there still seemed to be plenty of males to go round.
It occurred to me that these hybrids might be less healthy if they were growing in a natural situation, where they would be exposed to competition from other plants and to grazing by herbivores, rather than in the benign environment of the glasshouses. Perhaps the hybrids would be ravaged by slugs, or all their seeds would be consumed by campion moths, and this could explain why the two parent species did not blend together. I decided to set up a long-term field experiment. At the time Southampton University was fortunate to own a substantial country estate, Chilworth Manor, just to the north of the city. The manor had been converted into a rather posh hotel and conference centre – in fact I had been put up there when I was interviewed for the lectureship at Southampton. The grounds included a traditional Victorian walled garden, which was available for members of the biology department to conduct experiments, and extensive woodlands. I planted out replicate patches of both white and red campions, and their hybrid offspring, in woodland and in the open, sunny walled garden. My prediction was that the white campions should thrive in the open, and the red campions in the woodland. If the hybrids failed to thrive as well as the parents in either habitat, because they were poorly adapted to either habitat or because the hybrid populations became dominated by females, this could explain their relative rarity in the wild.