Evolution of Gall Morphology and Host-Plant Relationships in Willow-Feeding Sawflies (Hymenoptera: Tenthredinidae)

Abstract

Abstract. There are over 200 species of nematine sawflies that induce galls on willows (Salix spp.). Most of the species are mono-or oligophagous, and they can be separated into seven or eight different groups based on the type of gall that they induce. We studied the evolution of different gall types and host plant associations by reconstructing the phylogeny of five outgroup and 31 ingroup species using DNA sequence data from the mitochondrial cytochrome b gene. Maximum-parsimony and maximum-likelihood analyses resulted in essentially the same phylogeny with high support for important branches. The results show that: (1) the galling species probably form a monophyletic group; (2) true closed galls evolved only once, via leaf folders; (3) with the possible exception of leaf rollers, all gall type groups are mono-or paraphyletic; (4) similar gall types are closer on the phylogeny than would be expected by a random process; (5) there is an apparent evolutionary trend in galling site from the leaf edge towards the more central parts of the host plant; and (6) many willow species have been colonized several times, which excludes the possiblity of parallel cladogenesis between willows and the gallers; however, there are signs of restrictions in the evolution of host use. Many of the patterns in the evolutionary history of nematine gallers have also been observed in earlier studies on other insect gallers, indicating convergent evolution between the independent radiations.Key words. Coevolution, convergent evolution, evolutionary trends, extended phenotypes, gall morphology, gradualism, insect-plant relationships, Nematinae, phylogeny.Received June 1, 1999. Accepted October 11, 1999.The habit of galling has evolved many times independently in various organisms (Meyer 1987). In insects alone, gall induction has evolved in at least seven different orders, and in most of them several radiations have arisen (Meyer 1987; Dreger-Jauffret and Shorthouse 1992). The multiple origins of galling makes it possible to search for convergent features in these independent evolutionary histories. Indeed, recent phylogenetic analyses of gall-inducing aphids (Stern 1995), wasps (Stone and Cook 1998), and thrips (Crespi and Worobey 1998) have shown that common features exist in separate radiations. For example, in all these taxa gall morphology is determined mainly by the galler, not the host plant, and thus the gall can be considered an extended phenotype (sensu Dawkins 1982) of the galler.The nematine sawflies that induce galls on willows (Salix spp.) also offer a good model system for the study of evolutionary questions, especially questions about the evolution of different gall types and host plant associations (Price 1992). These sawflies belong to the tenthredinid subfamily Nematinae, which is comprised of hundreds of galling and nongalling species (Smith 1979;Gauld and Bolton 1988). There are about 200 species of galling nematines, most of which are mono-or oligophagous (Smith 1970;Price et al. 1994). Like their host plants, thes...

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.…”

“…Thus, our results indicate that the causes for the strict host specificity in gallers (2) are not linked to the chemical properties of the hosts; the reason may be in the ability to induce galls per se or in constraints (34,36) on the host recognition system. Because gall interior chemistry is not determined by the host plant, it is not surprising that no connection has been found between galler phylogeny and host plant chemistry in the few studies that have addressed the question (15,37). Indeed, it is likely that the factors determining the probability of host shifts in gallers are fundamentally different from those in other phytophagous insects, and thus studies on gallers can provide valuable new insights into the evolutionary interactions between plants and herbivores.…”

“…The nematines that induce true closed galls form a monophyletic group derived from species with folivorous larvae (15). Gall formation is initiated by the ovipositing female and, depending on the species, the feeding larva may stimulate its continued growth (16).…”

“…The gallers are closely related and belong to the monophyletic subgenus Eupontania Zinovjev, which includes species that induce pea-or bean-shaped galls close to the leaf midrib (15,16). In contrast, the host willows are chemically and taxonomically divergent, ranging from the creeping tundra species S. reticulata to the tree-like S. borealis.…”

Impact of the terminal Cretaceous event on plant–insect associations

“…We note that some occurrences of damage types within our generalized category undoubtedly represent feeding by specialist as well as generalist insects, thus biasing toward a conservative estimate for specialist extinction. Host specificity assignments were based on published surveys of modern plant damage linked to ecologically known insect taxa, including the spectra of host-plants consumed by descendant or otherwise related taxa (34)(35)(36), occasionally supplemented by plant-host specificity patterns observed in the fossils (24,37). Our determinations (Table 1) are an expansion of previous work characterizing insect damage on latest Paleocene to middle Eocene floras (27,30).…”