Not all aphids take the same risks

In 1970 an entomologist working on the black bean aphid, Aphis fabae, at Rothamsted Experimental Station (as it then was),  noted that he could categorise the winged individuals as either migrants, flyers or non-flyers; the former flying before they reproduced, the second flying after they reproduced and the final category, never flying (Shaw, 1970).  To describe this phenomenon he used the phrase “migratory urge” a term previously only used in the ornithological literature.

A few years later a group of PhD students in Tony Dixon’s lab at the University of East Anglia started dissecting aphids and counting their ovarioles, finding that unlike most other insects, ovariole number was variable within a species and not related to adult weight (Dixon & Dharma, 1980; Wellings et al., 1980; Leather, 1983).  Generally speaking, in insects, including aphids, the heavier they are, the more fecund they are, although in some instances this is not always true (Leather, 1988).

Figure 1 taken from http://www.aphidsonworldsplants.info/Cloning_Experts_3.htm

Figure 2 What aphid ovarioles really look like Dombrovsky  et al. BMC Research Notes 2009 2:185   doi:10.1186/1756-0500-2-185

What we found then (Wellings et al., 1980), and later (Leather et al., 1988), was that aphids with wings (alatae) even those from the same clone, had much more variability in the number of ovarioles contained within them than those without wings (apterae) (Leather et al., 1988), and that the more ovarioles an aphid contained the more fecund it was, although as mentioned earlier the number of ovarioles appeared to be independent of weight (Leather & Wellings, 1981).

So what does this have to do with migratory urge in Aphis fabae? In the early 1980s Keith Walters was working on migration in cereal aphids (Sitobion avenae and Rhopalosiphum padi) and discovered, that as with Aphis fabae these two species also produced alatae with different flight attributes (Walters & Dixon, 1983).  Building on what we in our group had discovered about ovarioles, Keith was able to show that the degree of migratory urge in aphids was determined by the number of ovarioles they contained. The greater the number of ovarioles the more reluctant they were to take flight (Figure 3ab).

Figure 3a Relationship between number of ovarioles and time to take-off (minutes) in Sitobion avenae  (Drawn from data in Walters & Dixon, 1983).

Figure 3b Relationship between number of ovarioles and time to take-off (minutes) in Rhopaloisphum padi  (Drawn from data in Walters & Dixon, 1983).

 He also found that the fewer the number of ovarioles, the steeper the angle of take-off was (Figure 4) i.e. aphids with few ovarioles climbed faster and more steeply and were thus more likely to end  up higher in the air, and thus more likely to travel further than those

Figure 4 Relationship between number of ovarioles and angle of take-off (degrees) in Rhopalosiphum padi (drawn from data in Walters & Dixon, 1983).

taking off at a shallower angle.  He also showed that resistance to starvation was greater in those aphids with fewer ovarioles and that they could also fly for longer periods of time.  Given that alatae of Aphis fabae also have a variable number of ovarioles, 6-12 (Leather et al., 1988), we can see that this fits in very well with Shaw’s classification of migrants, flyers and non-flyers.

This is yet another great example of the flexibility (plasticity) of the aphid clone.  By producing offspring that have different flight capabilities and propensities, the clone is able to hedge its bets in times of adversity; alate aphids in many aphid species are produced in response to crowding and/or poor nutritional quality (Dixon, 1973).  This deterioration in living conditions could be very local i.e. restricted to the plant on which the aphid is feeding or its immediate neighbours, slightly more widespread, i.e. at a field scale or at a much more widespread landscape scale.  Given that long distance aphid migration is very costly (only a tiny proportion survive, Ward et al, 1998) the best option is to spread the risk between the members of your clone.  Those individuals with more ovarioles and greater potential fecundity make the low risk short-distance hops (trivial flights), but take the chance that the next door plant might be just as bad as the one left behind and also within easy reach of natural enemies, but with a higher chance of arriving and reproducing.

A risk taking aphid!

 

At the other end of the scale, those clone members with fewer ovarioles and reduced potential fecundity make the long distance migratory flights, with the risk of not finding a suitable host plant in time, but with the chance that if they do, it will be highly nutritious and natural enemy-free.  A really good example of not putting all your eggs in one basket and yet again a demonstration of what fantastic insects aphids are 😉

 

References

Dixon, A.F.G. (1973) Biology of Aphids Edward Arnold, London.

Dixon, A.F.G. & Dharma, T.R. (1980) Number of ovarioles and fecundity in the black bean aphid, Aphis fabae. Entomologia Experimentalis et Applicata, 28, 1-14.

Leather, S.R. (1983) Evidence of ovulation after adult moult in the bird cherry-oat aphid, Rhopalosiphum padi. Entomologia experimentalis et applicata, 33, 348-349.

Leather, S. R. (1988). Size, reproductive potential and fecundity in insects: Things aren’t as simple as they seem. Oikos 51: 386-389.

Leather, S.R. & Welllings, P.W. (1981) Ovariole number and fecundity in aphids. Entomologia experimentalis et applicata, 30, 128-133.

Leather, S.R., Wellings, P.W., & Walters, K.F.A. (1988) Variation in ovariole number within the Aphidoidea. Journal of Natural History, 22, 381-393.

Shaw, M.J.P. (1970) Effects of population density on the alienicolae of Aphis fabae Scop.II The effects of crowding on the expression of migratory urge among alatae in the laboratory. Annals of Applied Biology, 65, 197-203.

Walters, K.F.A. & Dixon, A.F.G. (1983) Migratory urge and reproductive investment in aphids: variation within clones. Oecologia, 58, 70-75.

Ward, S.A., Leather, S.R., Pickup, J., & Harrington, R. (1998) Mortality during dispersal and the cost of host-specificity in parasites: how many aphids find hosts? Journal of Animal Ecology, 67, 763-773.

Wellings, P.W., Leather , S.R., & Dixon, A.F.G. (1980) Seasonal variation in reproductive potential: a programmed feature of aphid life cycles. Journal of Animal Ecology, 49, 975-985.

 

Not all aphids have wings

Given that aphids are commonly known as green-fly or black-fly, it might be presumed that all aphids are capable of flight. Although this is almost certainly universal at the species level (but see Post script) it is not true within a species. As I have described in an earlier post aphids are possessed of extremely complex and fascinating (to me at least) life cycles. Depending on the species, either most stages of the life cycle are winged (alate) as adults, e.g. the sycamore aphid Drepanoisphum platanoidis

I couldn’t resist showing you this beautiful picture of an adult sycamore aphid borrowed from the best aphid web site that I know of (see http://influentialpoints.com/Gallery/Drepanosiphum_platanoidis_common_sycamore_aphids.htm)

 

Other aphid species, such as my favourite, the bird cherry-oat aphid, Rhopalosiphum padi, only produce alate morphs at specific times of year or in response to changes in host plant quality or crowding.

  

Winged (alate) and non-winged (apterous) morphs of Rhopalosiphum padi.

In species such as the sycamore aphid, the only apterous morph tends to be the sexual female or ovipara, which has no need to disperse and after mating lives only long enough to develop and lay its eggs on the bark of sycamore trees.

Ovipara of the sycamore aphid searching for an oviposition site

In those species such as the bird cherry-oat aphid, the winged forms are very different from the non-winged forms, not just in terms of their wings but in their physiology, behaviour and life history traits (Dixon, 1998). The role of the winged morphs is to find new host plants and to start new colonies. They have long antenna, long legs and well-developed and many, sensory organs (rhinaria). They are the dispersal stage, or in the case of winged males, the mate seekers. They respond more readily to host odours; they need to be able to find new host plants at a suitable physiological stage and preferably free of natural enemies. A well-developed olfactory system is thus called for.

If you cut them open (preferably anaesthetizing them first), and remove their ovaries, you will find that they have ovarioles with only a few embryos in each chain and that most of the embryos are not mature i.e. without eye spots. In addition, if you cut open a number of individuals from the same clone you will find that they will not all have the same number of ovarioles. For example, the alate exules (winged forms produced on the secondary host plants )of Rhoaplosiphum padi, the number of ovarioles can range from four to ten (Wellings et al, 1980). This variability of ovariole number in the dispersal morphs of aphids that spend much of their life cycle on ephemeral host plants is quite common (Leather et al 1988).  So why do so many aphid species have variable numbers of ovarioles in their alate morphs?

Shaw (1970), showed that there appeared to be three types of black bean aphid (Aphis fabae) alate exules; migrants, those that flew before depositing nymphs, flyers, those that deposited a few nymphs before flying, and non-flyers, those that stayed and reproduced on their host plant. He postulated that this was an adaptation in response to host quality, the worse state the plant was in the more likely the migrant morph would be produced. Many years later Keith Walters and Tony Dixon (Walters & Dixon, 1983) were able to show that there was a very strong relationship between reproductive investment (number of ovarioles) and flight willingness and ability. The more ovarioles an aphid had, the less likely it was to want to take off and fly, and in addition those with more ovarioles could not fly for as long or as far as those with fewer.

In other words a trade-off between fecundity and migration. As long distance aphid migration is very costly (very few survive, Ward et al, 1998) it makes sense to have members of your clone spreading the load (risk), from short-distance hops (trivial flights), with the chance that the next door plant might be just as bad as the one left behind and within easy reach of natural enemies, but with a higher chance of survival and reproduction, to long distance migratory flights, with the reduced probability of finding a host plant but with the chance that it will be high in nutrition and low in natural enemies.

What clever beasts aphids are 😉

 

References

Dixon, A.F.G. (1998) Aphid Ecology, Second edn. Chapman & Hall, London.

Leather, S.R., Wellings, P.W., & Walters, K.F.A. (1988) Variation in ovariole number within the Aphidoidea. Journal of Natural History, 22, 381-393.

Shaw, M.J.P. (1970) Effects of population density on the alienicolae of Aphis fabae Scop.II The effects of crowding on the expression of migratory urge among alatae in the laboratory. Annals of Applied Biology, 65, 197-203.

Walters, K.F.A. & Dixon, A.F.G. (1983) Migratory urge and reproductive investment in aphids: variation within clones. Oecologia, 58, 70-75.

Ward, S.A., Leather, S.R., Pickup, J., & Harrington, R. (1998) Mortality during dispersal and the cost of host-specificity in parasites: how many aphids find hosts? Journal of Animal Ecology, 67, 763-773.

Wellings, P.W., Leather , S.R., & Dixon, A.F.G. (1980) Seasonal variation in reproductive potential: a programmed feature of aphid life cycles. Journal of Animal Ecology, 49, 975-985.

 

Post script

It is possible that there are some aphids that never fly – Aphids from the genus Stomaphis have incredibly long mouthparts (they all feed through tree bark), and as far as I can tell from perusal of

Roger Blackman and Vic Eastop’s monumental work, alate morphs have never been described (or seen) and even males are apterous.

Blackman, R.L. & Eastop, V.F. (1994) Aphids on the World’s Trees. CABI, Wallingford.

 

Post post script

For a very detailed and thoughtful review of the ‘decisions’ and costs involved in aphid reproductive and dispersal biology see Ward, S.A. & Dixon, A.F.G. (1984) Spreading the risk, and the evolution of mixed strategies: seasonal variation in aphid reproductive strategies. Advances in Invertebrate Reproduction, 3, 367-386.

 

Living inside your grandmother – the wonderful world of aphids

How many of you realise that when you look at an aphid you are simultaneously looking at first, a clonal organism and secondly a mother, her daughter and her granddaughters, all housed in the same body?  This is the wondrous phenomenon known as telescoping of generations.  Aphids, except just before overwintering, give birth to live young (viviparity), and without the need of a male (asexual reproduction/parthenogenesis).  Thus for most of the time when you look at an aphid, you are looking at one member of a clone i.e her sister-self-daughter.  Not only that, but you are looking at not only the aphid in front of your eyes, but at her daughters and her daughter’s daughters, all of which are neatly lined up in tidy rows within the ovarioles of their respective mothers.  With aphids, it is not just maternal effects you have to consider, but also grand-maternal effects, so any experiments should take into account the host-plant and environmental conditions that the ‘grand-mother’ experienced, not just those of the ‘mother’.

Reproduced from Dixon (1973)

In addition, as the eggs are hatched within the aphids before they are born, their total development time, compared with those insects that lay eggs which hatch externally to their mothers, is significantly reduced, thus giving them a head-start in the population development race.  This is suggested as one of the reasons why aphids are so successful as pest insects.

Generally speaking, this wonderful world of internal generations is hidden from us, unless we cruelly dissect the clone mother and extract her ovarioles.  In some aphids however, such as the small willow aphid, Aphis farinosa, where the offspring are a completely different colour from their mother, the next generation of aphids becomes clearly visible without the need to cut open the mother.

And before you ask, as far as I know, there is no evidence that the generations within a generation go on ad infinitum, like a hall of mirrors, although it would be really cool if they did.

No wonder I love aphids so much.

Dixon A.F.G. (1973)  The Biology of Aphids, Edward Arnold, London

P.S. Tony Dixon’s little Biology of Aphids book is a great introduction to the subject, unfortunately out of print, but the good news is that it is still possible to buy second-hand copies for less than £5. Another great and very readable book, is Aphid Ecology, also by Tony and again out of print, except as an e-book.  The really bad news is that the cheapest copy I have been able to find is priced at £43.31 prior to shipping, so if you want to read it the best option is to borrow it from the library.