TRENDS in Ecology & Evolution Vol.17 No.5 May 2002 http://tree.trends.com 0169-5347/02/$ – see front matter © 2002 Elsevier Science Ltd. All rights reserved. PII: S0169-5347(02)02486-2 199 Research Update Aphids hold a special place in the study of social evolution, because they include the only eusocial animals that are clonal. We might expect social aphid colonies, if they consist of pure clones, to be free from reproductive conflict. A fascinating new study by Abbot and colleagues shows that there can be high levels of clonal mixing within colonies of a social aphid. The intruding aphids cheat on the host clone by not helping in gall defence and instead invest singlemindedly in growth and reproduction. Now that aphid soldiers have been shown to cheat, as well as to defend, clean and repair their galls, it is perhaps time to admit them ungrudgingly to the elite cadre of the truly social insects. Published online: 6 March 2002 Aphids would seem to be the epitome of defencelessness. Small soft cushions of haemolymph, they huddle on leaves and stems, ready to be ripped apart by ladybirds, sucked dry by lacewings, hoovered up by hoverflies and punctured by wasps. The discovery that certain species have aggressive soldiers therefore came as a surprise: nobody ever expected the soft cushions to fight back [1]. Soldier aphids are rare (only ~1% of the 4500 species have them) but they are impressively diverse in the weapons and behaviour that they use [2], and they have evolved independently ~17 times (T. Fukatsu, pers. commun.). The distinguishing feature of aphid societies is that, provided they comprise a pure clone, there should be no reproductive conflict. In all other societies, there is inevitably conflict among individuals, because they are not all equally related to each other’s offspring. However, the assumption that social aphids live in pure clonal groups has never been properly tested. This is what Abbot et al. have done [3]; they have shown that the clones do mix, and with fascinating consequences. They studied the aphid Pemphigus obesinymphae, which form long-lived galls on cottonwood Populus trees in North America [4]. The genus Pemphigus occurs throughout the North Temperate region (including the UK) and includes several soldier-producing species [3]. Individual females, which we can legitimately call ‘queens’, make a globular gall on the leaf, in which they asexually produce up to 300 first-instar soldiers. The P. obesinymphae queen cannot escape from the gall, but the soldiers can come and go through a small ostiole. This hole is the Achilles Heel of the gall: it is essential for the aphids to get rid of their waste products (honeydew) [5], but it is also large enough to allow predators to get in and eat the queen. The gall remains in this condition for several months, during which time the soldiers effectively, and often suicidally, defend their home from attack by predators that can be much larger than them (Fig. 1). At the appropriate time, the soldiers resume their development and mature into winged aphids that leave the gall and fly to another, herbaceous, host plant. Abbot et al. have shown, by direct observation, that soldiers leave their natal galls in appreciable numbers and infiltrate other galls inhabited by aphids to whom they are not at all related. The authors used aphids marked with coloured powders and by using sticky bands on the twigs: some aphids were able to walk nearly 2 m. They also used genetic markers [single-nucleotide polymorphisms of the aphid bacterial endosymbiont Buchnera, and multilocus intersimple sequence repeats (ISSR) on the aphids themselves] to reveal that the level of clonal mixing was high. In seven galls analysed by ISSR, on average 38% of the aphids were from alien clones and five of the seven galls contained intruders from more than two other galls. Although this is a small sample from a restricted locality, it is clear that soldier behaviour can be maintained in an aphid species even when the level of clonal mixing is high. Even more interesting than this demonstration of extensive clonal mixing, are the results of their experiments on how the intruding aphids behave. Abbot et al. inserted Drosophila larvae into natural galls and, after a few minutes, removed them, together with the soldier aphids that had attacked and were still stuck to the larvae. They then genotyped all the aphids that had been in the gall and found that the intruder aphids were far less likely to attack the fly larva. Although ~36% of the aphids in the gall were intruders, only 2% of the attacking aphids were not native to the gall. Clearly, the alien aphids had decided to let the native soldiers take care of gall defence. Furthermore, the intruding aphids do not spend much time as first instars, but accelerate their development into winged adults that leave the gall to reproduce on other hosts. Although this kind of selfish behaviour is exactly what one would expect on the basis of kin selection theory, it is nevertheless a remarkable result. It means that the aphid clones have a condition-dependent altruistic strategy. In your own gall, you should grow slowly and be prepared to fight. But if you have dispersed to another gall, cheat on your new mates, do not risk your life attacking, but develop and leave the gall as quickly as you can. It would be interesting also to know whether the intruders shirk on the normal housekeeping duties of soldier aphids. The vital task of pushing Soldier aphids go cuckoo William A. Foster Fig. 1. First-instar soldier aphids attach a fly larva on the surface of a gall of Pemphigus obesinymphae. Gall diameter is ~1.6 cm. Note exit hole of gall just to the right of the larva. Photograph reproduced with permission from Patrick Abbot. Research News