The Masters of Cloning

Aphids are the cloning experts. A few yards from your door there may be hundreds of these tiny insects, sucking away at the roses or the clematis, and all busy making identical copies of themselves. They have, moreover, more than 160 million years’ experience of cloning, more than 160 million years in which evolution and natural selection have enabled them to overcome the problems and exploit all the advantages of clonal reproduction. Here we will explore how they do it.

To most people, aphids are just pests. The greenfly, blackfly or plant-lice of farm and garden can cause serious damage to crops by the sheer weight of their numbers, or by spreading virus diseases of plants, in much the same way as mosquitoes spread malaria. Colonies of thousands of individuals can appear on plants in a few days, as if by magic. This phenomenal rate of reproduction is only possible because no time or energy is wasted on sex. All the aphids in these colonies are female. Dispense with males and there is no need to expend time and energy on finding mates, courting, and the laying and incubation of eggs. Parthenogenesis ˗ the development of unfertilised eggs ˗ enables female aphids to give birth as soon as they are adult. Their progeny are born alive and kicking like human young, but nothing like so helpless, and what is more they are all female, ready in a matter of days to give birth themselves.

To understand and appreciate the aphid way of life we have to look at every aspect of it, and search for the answers to the numerous questions that arise. How do the eggs develop without being fertilised, and how do all the offspring develop as females? Do populations of aphid clones respond to changes in their environment differently from populations of most other forms of life, where every individual is unique? How do they interact with other organisms, including the plants on which they feed? The extraordinary powers of multiplication unleashed by parthenogenesis could within a year produce a layer of aphids about 150 km deep over the entire surface of the earth, if they were allowed to go unchecked (Harrington 1994). Obviously it is not in the aphids’ own interests to realise this full potential, or even the minute fraction of it that would cause them to over-run their host plants. So they have developed their own means of restricting population growth, by interacting with one another, rather than relying on external agencies such as the weather and natural enemies. It is like having an immensely powerful car, capable of almost infinite speeds when overtaking or eating up the open road, but useless and dangerous without efficient means of braking and speed regulation.

Populations that reproduce clonally can more readily evolve mechanisms for restricting their own population growth, because it is the survival of the clone that matters, not that of any one individual. In the world of aphids, natural selection acts on clones, and the individual is of little consequence, so thousands of individuals can be sacrificed as long as the clone survives to perpetuate its particular genetic constitution (its genotype). An aphid clone is in this sense a “super-individual”, with all its parts – the individual aphids – acting in support of the whole. During the course of its life a successful clone may disperse over a large area, so that the “super-individual” becomes a diffuse organism that mortality factors acting at any one time or place are unlikely to kill.

There is another important advantage of being a “super-individual”. All its individual aphid parts do not have to do the same thing. Just as genes may be switched on or off during the development of an organism to produce organs with different bodily functions, individual aphids can be induced to develop in different ways resulting in different forms or phenotypes, with different roles to play in the life of the clone. The two most important of these roles are feeding and dispersal. Feeding aims at converting plant biomass into aphid biomass as quickly and efficiently as possible, and as any one aphid can only grow to a certain size, feeding is linked to rapid multiplication. Dispersal means spreading the clone around and, as most aphids are very fussy about what they eat, this also involves finding the right host plant. These two basic roles differ fundamentally. The feeding and multiplication role requires an aphid to spend all its life sucking plant sap and devote all its energy to motherhood. A body specifically designed to fulfil such a role would be a wingless, sedentary, membranous sac, with most of the body cavity occupied by developing embryos, to which it continuously gives birth. The dispersal and host-finding role requires an active winged insect with its thoracic skeleton and musculature fully developed to provide the power for extensive flight, and the appropriate sense organs and behavioural systems to enable it to recognise and respond to a host plant.

Fig. 1. Wingless and winged parthenogenetic females of the peach-potato aphid, Myzus persicae

The ability of aphid clones to produce both wingless and winged forms is therefore fundamental to the way of life of most aphids, although the details of how and when they are produced vary between species. And inevitably there have to be some compromises. Wingless aphids are rarely completely sedentary as they usually have to fulfil other requirements such as the ability to change their feeding position and to protect themselves from natural enemies. Winged aphids have not only to find new hosts but to establish new colonies, so they need to have developing embryos inside them and give birth soon after they have completed their flight.

The ability to produce different phenotypes for different purposes is particularly important to aphids that have host alternation. Many aphids in temperate regions of the world spend the winter on a woody plant – a tree or shrub – and produce colonies on the expanding buds and leaves in spring, making full use of the first flush of spring growth. Winged females are then produced which migrate to a secondary host, usually a rapidly growing herbaceous plant, where their clone can again for a short time realise its full reproductive potential. Eventually, usually in the early autumn, winged migrants return to the woody plant again. Host alternation has evolved several times independently in aphids, and is clearly a very successful way of spending as much of the year as possible on actively growing plants. But it would not be possible without clonal reproduction, for two reasons. First, the migration to and from the woody host is an extremely hazardous procedure for a small flying insect, and must involve the production and sacrifice of many winged individuals, in order for a few to find the right host plants and enable the survival of the clone. Second, it involves the individuals of the clone not just in two roles – flight and feeding – but in others associated with the change of host plant. The wingless forms feeding on a woody host require different specialisations from those feeding on a herbaceous plant, and the winged forms that leave the woody host to find the right herbaceous plant for their clone to feed on have different sensory and behavioural mechanisms from those that later make the return migration to the woody host.

The interactions between the individuals of an aphid clone and the allocation of different tasks to different phenotypes are a form of social behaviour. Sociality in insects is based on relatedness. In bees the workers co-operate to maintain the hive because they are sisters, sharing half their genes and therefore with a strong interest in ensuring the colony’s survival. The aphids in a clone have all their genes in common, and therefore the ties that bind them and the selection for co-operative behaviour are even stronger. We have already noted the altruism of winged migrant aphids, thousands of them taking off into the unknown to find new host plants. The individual aphids in colonies on plants undoubtedly interact with one another by touching and by chemical communication using pheromones, but a free-living colony may often consist of a mixture of clones, in which case competition may be as or more likely than co-operation. For real social behaviour in aphids one needs to look at the clonal colonies that develop within the closed, controlled environments of galls. Several groups of aphids induce the actively-growing tissue of their host plant to form a closed gall, inside which hundreds or thousands of their offspring can develop. The inhabitants of these galls have in some species developed elaborate social systems, with soldiers to defend the gall, and tasks allocated to other inhabitants such as keeping the inside of the gall clean or repairing any damage. The degree of sophistication shown by these aphids is on a par with that of bees, ants and termites, and may be somewhat surprising when contrasted with the superficially primitive-looking aphid masses on the plants in one’s garden.

One crucial point about the biology of aphids has not so far been mentioned. Once every year, most aphid species have sex. Some have sex only once every two years. A small number of species, including some that are world-wide pests, appear to have given up sex altogether, and reproduce continuously by parthenogenesis from year to year. But as we get to know them better we are discovering that we may simply not have been looking hard enough, and that even these species may not be as sexless as they seem. Pest aphids have spread themselves far and wide in very recent times with the growth of modern agriculture, and clonal reproduction is obviously the best way to exploit the very unnatural environment provided by the crops that we grow. Back where they came from, in their natural environment, these species may still be having sex on a regular basis.

So, aphid clones do not go on reproducing themselves indefinitely. In fact studies have revealed that aphids have developed an elaborate system for detecting seasonal clues and making developmental switches, to ensure that after a certain time clonal reproduction ceases and that radically different sexually-reproducing forms – the males and egg-laying females – make their appearance, mate and produce fertilised eggs. Although aphids have been cloning themselves for more than 160 million years, and despite having developed ways of exploiting all the advantages that clonal reproduction can provide, sex apparently still has an important part to play in their lives. The question “What use is sex?” has exercised the minds of biologists for many years. Perhaps aphids can help to lead us towards an answer.

Fig. 2 Male and egg-laying female of the peach-potato aphid (Myzus persicae) mating.

Harrington, R. (1994) Aphid layer. Antenna 18: 50-51.