The structure of cynipid oak galls: patterns in the evolution of an extended phenotype

Abstract

Galls are highly specialized plant tissues whose development is induced by another organism. The most complex and diverse galls are those induced on oak trees by gallwasps (Hymenoptera: Cynipidae: Cynipini), each species inducing a characteristic gall structure. Debate continues over the possible adaptive signi¢cance of gall structural traits; some protect the gall inducer from attack by natural enemies, although the adaptive signi¢cance of others remains undemonstrated. Several gall traits are shared by groups of oak gallwasp species. It remains unknown whether shared traits represent (i) limited divergence from a shared ancestral gall form, or (ii) multiple cases of independent evolution. Here we map gall character states onto a molecular phylogeny of the oak cynipid genus Andricus, and demonstrate three features of the evolution of gall structure: (i) closely related species generally induce galls of similar structure; (ii) despite this general pattern, closely related species can induce markedly di¡erent galls; and (iii) several gall traits (the presence of many larval chambers in a single gall structure, surface resins, surface spines and internal air spaces) of demonstrated or suggested adaptive value to the gallwasp have evolved repeatedly. We discuss these results in the light of existing hypotheses on the adaptive signi¢cance of gall structure.

Are gall midge species (Diptera, Cecidomyiidae) host-plant specialists?

“…Related galling insect species usually induce morphologically similar galls on phylogenetically related host plants . Phylogenetic evidence also suggests that gall morphology of aphids (Stern 1995;Inbar et al 2004), thrips (Crespi & Worobey 1998;Morris et al 2002;McLeish et al 2006), sawflies and gall wasps (Stone & Cook 1998;Stone et al 2002;Cook et al 2002) is controlled by the gall inducing organism.…”

Manipulation of the phenolic chemistry of willows by gall-inducing sawflies

“…Recent phylogenetic analyses of gall-inducing aphids (21), cynipid wasps (22), thrips (23), and sawflies (15) have shown that the insects, not their host plants, determine the location, size, and shape of galls. Thus, gall morphology can be regarded as an extended phenotype [sensu Dawkins (24)] of the galler.…”

Diversity of galls induced by wasps (Hymenoptera: Cynipidae, Cynipini) associated with oaks (Fagaceae: <em>Quercus</em>) in Mexico

“…Nearly a thousand species of gall-inducing wasps have been reported (Hymenoptera: Cynipidae: Cynipini) in oak species (Fagaceae: Quercus) (Kinsey 1936, Weld 1960, and they are among the most structurally complex and diverse galls (Liljeblad et al 2008). Gall structures reflect the primary characteristics of the insect inducer, representing an extension of their phenotype (Stone & Cook 1998). The host species of the Cynipini are almost exclusively limited to the Quercus genus (Liljeblad et al 2008), although some use other hosts within the Fagaceae family, such as Castanea, Castanopsis, Lithocarpus and Chrysolepis (Nieves-Aldrey 2001, Stone et al 2002, Liu & Ronquist 2006.…”

“…During each generation, cynipid species have the ability to induce specific and complex galls on oaks, and in the majority of cases, they form a different gall morphotype each generation (e.g., sexual and asexual). Another characteristic in some species of cynipids is host alternation (heteroecy), which occurs every generation (Askew 1984, Cook et al 1998.…”