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10. Galls and the evolution of social behaviour in aphids W.A. FOSTER and P.A. NORTHCOTT Department of Zoology, University of Cambridge, Downing Street, Cambridge, UK Abstract In several aphid species there is a soldier caste that actively defends the aphid colony. All the aphids that produce soldiers belong to species that induce galls on their host plants. Gall formation and soldier production are restricted to two of the families within the Aphidoidea—the Hormaphididac and the Pemphigidae. Information about the behaviour of the species (approximately 30) in which soldiers have been described is summarized. The paper examines how living in a gall might affect the social organization of aphids and increase the likelihood of the production of soldiers and the evolution of cooperation. The argument is proposed that the gall is important in providing a resource that can be readily defended and kept clean. In addition, the gall is important in providing a ring-fence around the clones, increasing the likelihood that aphids are related to their close neighbours. Soldier production might be encouraged in those galls that are relatively long- lived. Introduction It is now well-established that several aphid species are organized into societies that are defended by a specialized soldier caste (for example, Aoki 1977a; Itô 1989; Foster 1990; Kurosu and Aoki 199la). These aphids are of interest to evolutionary biologists because they provide a new group in which to investigate the evolution of altruistic behaviour. The most widely applicable explanation for the evolution of altruism is Hamilton’s (1964) idea of kin selection: an individual will be selected to value the reproduction of another according to how closely the two individuals are related. This is usually expressed in terms of Hamilton’s Rule, which gives the conditions under which a gene for altruism might Plant Galls (ed. Michèle A. J. Williams), Systematics Association Special Volume No. 49, pp. 161-82. Clarendon Press, Oxford, 1994. © The Systematics Association, 1994. 162 W.A. Foster and P.A. Northcott be expected to spread in a population (Grafen 1991). Imagine a donor provides help to a beneficiary, which incurs costs (c) to the donor and benefits (b) to the beneficiary. This helping behaviour will be selected for if the following inequality is satisfied: b/c>r (donor to own offspring)/r (donor to beneficiary’s offspring) (10.1) where b is the increase in the number of the beneficiary’s offspring as a result of the helping behaviour of the donor, c is the decrease in the number of the donor’s offspring as a result of her helping behaviour, and r is relatedness. Since aphids are parthenogenetic, an aphid colony has the potential to be a pure done, in which all the individuals are related to each other with a value of 1. Hamilton’s rule is then simple to apply: as long as b exceeds c, altruism will be selected for. Therefore, in clonal organisms the genetic predispositions for helping behaviour are high: in a pure clone, barring mutation, there is the certainty (rather than probability) that the relatedness between two individuals, no matter how distant genealogically, is 1. Aphid soldiers and the gall-forming habit Soldiers have been described in species from two aphid families: Hor- maphididae and Pemphigidae. (We are following here the classification of Heie (1980); see also Ilharco and van Harten 1987). We are using here a broad, behavioural definition of ‘soldier’: any set of individuals that act defensively with some likely fitness loss to themselves will be considered to be soldiers. Several authors have used a more restrictive definition, with the requirement that soldiers should be sterile (for example, Aoki 1982a: Ito 1989). However, social insect castes are usually defined in terms of their behavioural roles (for example, Holldobler and Wilson (1990); but see also Peeters and Crozier 1988): therefore, we will refer to all sets of aphids with well-defined defensive behaviour as soldiers, whether or not they have been shown to be sterile and whether or not they are morphologically distinct from non-defensive individuals. All of the aphid species that have soldiers also form galls on the primary host or are from gall-forming genera, in the case of species whose primary host is not known (Table 10.1). Indeed, true gall-forming species are almost entirely restricted to the Hormaphididae, Pemphigidae, Adelgidae, and Phylloxeridae (Wool 1984). (The last two families are generally regarded as belonging to the non-aphid superfamily, Phylloxeroidea.) The broad purpose of this contribution is to establish whether there is any biological significance in the fact that all the soldier-producing aphids The evolution of social behaviour in aphids 163 are also gallformers. Does the gall-forming habit in some way predispose the evolution of soldiers and eusociality in aphids? In this paper, we will briefly describe the different types of soldier aphids, their taxonomic distribution, and whether or not they live in galls. We will then ask how, in terms of Hamilton’s Rule, the gall-forming habit may have been an enabling factor in the evolution of social behaviour in aphids. The association between the gall-forming habit and soldier production Table 10.1 shows the relationship between gall forming and soldier production in the major groups of aphids. At first glance, it seems to provide an indication that this relationship is firm: all the genera of aphids with soldiers are from gall-forming taxa and the vast majority of aphids that do not produce soldiers also do not form galls. However, there are at least three reasons for thinking that this association is not as secure as the table might seem to imply. First, in order to make any kind of claim about the correlation between two traits in a group of organisms, it is essential to have some idea about how often the traits have evolved independendy and for this a knowledge of the phylogeny of the organisms is required (for example, Ridley 1983; Harvey and Pagel 1991). Clearly, if gall forming and soldier production arose independently in each of the soldier-producing genera, this is a much stronger case for the biological significance of the association than if the two traits evolved only once, for example, in the common ancestor of the Hormaphididae and Pemphigidae. However, as far as we know only one cladogram of the Aphidoidea has ever been attempted (Heie 1987) and there are no published accounts of the cladistic relationships within the Hor maphididae and Pemphigidae. Secondly, soldier behaviour has been looked for in only a very small number of aphid species. Undoubtedly, many more aphid species with soldiers await discovery. Finally, in some species, the soldier morphs are on the secondary host, where galls are not usually found, and it is not clear whether these cases should be cited as evidence for an association between gall forming and soldier production. Aphid galls in relation to the life cycle The life cycles of the two gall-producing aphid families are very similar. There is an alternation of hosts between a primary host, on which the sexuals mate and lay an egg, from which the fundatrix hatches and forms 164 W.A. Foster and P.A. Northcott Table 10.1. Gall-forming and social aphids Taxon Gall Genera in which defender No. of forming morphs are species (a) known (b) not known in the taxon Phylloxeroidea Adelgidae Yes None All 47 Phylloxeridae Yes None All 69 Aphidoidea Lachnidae Chaitophoridac Drepanosiphonidac“ Aphididac4 ■ No None All 3323 Greenideidae Phloeomyzidae Anoeciidae Thelaxidae Hormaphididae 171 Cerataphidinac Yes Aleurodaphis 81 Astegopteryx Cerataphis Ceratoglyphina Ceratovacuna Pseudoregma Tuberaphis Nipponaphidinae Yes Nipponaphis 82 Hormaphidinae Yes Hamamelistes 8 Hormaphis Pemphigidae 266 Eriosomatinac 63 Eriosomatini Yes Eriosoma Schizoneura Tetraneurini Yes Colophina Tetraneura Hemipoda.ph.is Kaltenbachiella Pcmphiginae 146 Prociphilini Yes Pachypappa Pachypappella Gootiella Prociphilus Pemphigini Yes Pemphigus Thecahius Fordinac 57 Fordini Yes Aploneura Forda Baizongia Melaphidini Yes Melaphis “ One genus Tamalia is gall forming and is accorded sub family status by some authors (Remaudiere and Stroyan 1984). b Two genera Tuberocephalus and Eumyzus have one or more gall-forming species. The evolution of social behaviour in aphids 165 a gall, and the secondary host, where successive, entirely parthenogenetic, generations of females develop (Fig. 10.1a). Winged gall emigrants fly from the primary to the secondary host and winged sexuparae travel from the secondary to the primary host, transporting the sexuals inside them; for example, Foster and Benton (1992). The primary hosts of each of the major subgroups of these two families are usually woody and tend to be highly conserved: for example, the Pemphigini form galls on species of Populus, the Cerataphidinae on Styrax, the Melaphidini on Rhus, and the Fordini on Pistacia. The secondary hosts used by the species in each subgroup tend to be very diverse and for this reason it is argued that the association with the primary host is older than that with the secondary host (for example, Heie 1980). The Prociphilini provide an exception: the sexuals, egg, and fundatrix live on a range of woody angiosperms and the other parthenogenetic generations occur on the roots of Pinaceae (Moran 1992). There are important variations on this basic life cycle in these two families. Some species remain all year on the primary host (monoecious): the winged aphids that leave the gall are sexuparae that migrate to another part of the primary host, for example, the bark, where they give birth to the sexuals (Fig. 10.1b). Other species have lost the sexual phase, and remain all year on the secondary host (anholocyclic). The genus Pemphigus in Britain provides clear examples: most species alternate between galls on Populus and the roots of herbaceous secondary hosts, but Pemphigus spyrothecae remains all year on the primary host and Pemphigus saliciradicis is anholocyclic on the roots of Salix. Other examples are given in Table 10.2. Some aphid genera, for example, members of the Fordini, show the usual alternation of generations in parts of the world where the primary hosts (Pistacia) occur, but are anholocyclic on the secondary host in areas where the primary host is not found, for example, in Northern Europe. With this background we will now consider the types of soldier that are found and the number of times that the soldier habit might have evolved. How often has soldier behaviour evolved? It is generally accepted that the Hormaphididae and the Pemphigidae are closely related. They share several apomorphic characters (Heie 1987), but the Anoeciidae may belong to the same monophyletic group, perhaps being more closely related to the Pemphigidae than the Hor maphididae (Heie 1987). They are both probably rather ancient groups, whose habits, for example, gall formation and their host associations and life cycles, were fixed a long time ago. Gall formation was therefore 166 WA. Foster and PA. Northcott LIFE CYCLE OF PEMPHIGUS BURSARIUS Poplar bark WINGED SEXUPARA WINGLESS SOIL VIRGIN WINGED GALL EMIGRANT Poplar gall Fig. 10.1. Life cycles of Pemphigid aphids, (a.) Life cycle of Pemphigus bursarius, (b.) life cycle of Pemphigus spyrothecae. The dense stippling indicates the time spent in the gall, the lighter stippling indicates the time spent on the secondary host. Dark-headed arrows indicate ‘gives birth to’, light-headed arrows ‘grows up into’. probably a feature of the common ancestor of these two families and would have been a shared derived character if the more ancient aphids from which they evolved did not form galls. It could also be argued, in a similar way, that soldier production is a shared feature of the two families and evolved on only one occasion. This seems highly unlikely. However, given our ignorance about the cladistic relationships of the The evolution of social behaviour in aphids 167 (b) LIFE CYCLE OF PEMPHIGUS SPYROTHECAE Poplar bark MALES WINGED SOLDIERS NON-SOLDIERS V WINGLESS GALL VIRGIN Poplar Gall taxa within the Hormaphididae and Pemphigidae and about the true extent of soldier behaviour, we should not be too dogmatic. The best evidence that soldier behaviour has evolved more than once is provided by the morphology and behaviour of the soldiers themselves. Table 10.2 shows all the records of soldier behaviour that we have been able to extract from the literature and Table 10.3 categorizes aphid soldiers into four main types. These correspond approximately to the categories proposed by Aoki (1987) and Ito (1989). Within the Pemphigidae, there have probably been at least two independent origins of soldier behaviour. In the Colophina-type, the soldiers on the secondary host are first instars and for weapons they use their stylets and their enlarged and sclerotized fore and mid-legs. In some species (for example, C. clematis), the soldiers are sterile and distinct in morphology from the normal first-instars (‘dimorphic’) and in others (for example, C. clematicola), all the first instars are soldiers and can develop into fe o ■a. ja o d "S'! • a R .<3 <35 § r. •a, W§ S« Ss -S2? -22 sta ~Ci -2 ~^2 ^ n rs ^ ^ i wX <-■coft. <■3t" r■N|a <<S«3i J|^2fS jS^<3 s _^Jg ^^as _g^: instar. the same me of sas d e- Jf3r the aphi X .■.*5°Efl , '-^cS . 7gos5C5 'S^«Voc5 «t\o£g§j *j:vojc _.P5PC- oc £ 'c ■fs§Cr 'o!S« egcc- ^11o ve) occur in from other Q ^P Z S z Q c/5 S lS z S z nsict en defdisti is oldiers Coaa -“c^acOæaJ' jfyC/tÎ 3 TTm£CoO33 "TccJ -c&a Xo m& m& m& ms (one of which ot morphologically s orn f of aphid ological nders are types T£cC3Gz fc- fo3c' XC0!3 £03 £03r ’Vcc03o morphhe defe chief Xo o OT£h •c£cu inOÜo •G£ e o at two that t he thns T ans mea e Table 10.2. o ®.■1Ng=, =b033e “ Dimorphic mMonomorphic The evolution of social behaviour in aphids 169 reproducing adults (‘monomorphic’). Colophina-type aphids also produce soldiers in the gall on the primary host: these are usually second instars, but they use the same weapons as the secondary host soldiers and they are not sterile. It is likely that the soldiers on the primary and secondary host are homologous and represent a single origin of soldier behaviour. The sterile, dimorphic soldiers on the secondary host are probably the most derived type of soldiers in this group. The Pemphigus-type soldiers all occur in galls on the primary host: they use their stylets and hind-legs as weapons and none of them is sterile. In one species, Pemphigus spyrothecae, the first instars of the same generation are dimorphic (Lampel, 1968—1969), but both the soldiers and the normal 1st instars are able to moult to the next instar (Aoki and Kurosu 1986; Foster 1990). The soldiers produced towards the end of the season are probably functionally sterile, since they will not have time to develop into sexuparae before leaf fall. The soldier behaviour observed by Akimoto (1983) in Eriosoma moriokense may represent a third independent origin of soldier behaviour in the Pemphigidae. He observed the second and third instars, which are not sterile, behaving defensively, using their stylets. At least two distinct types of soldier are found in the Hormaphididae. The first type, the horned soldiers, occur on the secondary host (typically a grass, such as bamboo): they are first instars with greatly thickened forelegs armed with strong claws, they have strongly sclerotized tergites, and the frontal horns are sharp and well-developed. Two genera are involved: all the species of Pseudoregma appear to have a morphologically distinct soldier caste, but in at least one of the Ceratovacuna species ('C.lanigera) the soldiers are monomorphic and are not sterile. The second type is confined to galls on Styrax, the primary host and we have named them the .S'/}!raA'-gall-typc of soldier. They are typically sterile, dimorphic, second instars using their stylets as weapons (the aphids on the primary hosts do not have frontal horns). They also have stout spines on the head (four in Astegopterpx, two in Cerataphis fransseni). The legs are not especially well-sclerotized. Some species (for example, possibly Pseudoregma koshunensis) may produce both types of soldier during their life cycle. Aoki (1987) argues that these two types of soldier, even if they occur in the same species, are not homologous and represent independent origins of soldier behaviour. Part of the evidence for this is the different morphology of the two types of soldiers: those on the primary host are second instars and attack predators with their stylets, those on the secondary host are first instars and pierce predators with their frontal horns. However, in some Styrax aphids there are soldier first instars (called ‘outsiders’ by Kurosu and Aoki 1988a), so the instar distinction is probably not fundamental. Further support for the idea that the two types of soldiers are distinct is the fact that it is possible to build up a Table 10.3. Aphid species in which soldier behaviour has been observed Species Primary host Gall Secondary host Primary host Secondary host References soldiers" soldiers" Hormaphididae Cerataphidinae Aleurodaphis Styrax japonica Broccoli-shaped II, sterile, di Unknown Aoki and Usaba takenouchii styl, morph (1989) (Takahashi) Astegopteryx Styrax suberifolia Banana-bundle Bamboos II, sterile, di I, not sterile, mono Aoki and Kurosu bambucifoliae Dendrocalamus styl, exp styl, obs (1989a,c,d), Kurosu (Takahashi) Bambusa, etc. and Aoki (1991a) styraci Styrax obassia Coral-like Monoecious II, sterile, di Aoki and Kurosu Matsumura styl, exp (19896, 1990) Cerataphis fransseni Styrax benzoin ‘Bud gall’ II, sterile, di Noordam (1991) (Hille Ris styl, obs Lambers) Ceratoglyphina Styrax suberifolia Cauliflower Bamboo II, sterile, di Unknown Aoki et al. (1977), bumbusaf van (Pleioblastus) styl, exp Aoki (1979a), Aoki der Goot and Kurosu ( 1989<7), Aoki et al. (1991), Kurosu and Aoki (1991V) Ceratovacuna floccifera Bamboo I, sterile(?), di Noordam (1991) Noordam horns, fl, morph japónica Styrax japonica Cat’s-paw Bamboos II I, sterile, di Aoki et al. (1981), (Takahashi) Pleioblastus chino horns, fl, obs Aoki (1987), Aoki and Kurosu (1989a), Kurosu et al. (1990), Aoki and Kurosu (19916)