Behavioural, ecological and genetic evidence confirm the occurrence of host-associated differentiation in goldenrod gall-midges.

Host-associated differentiation (HAD) is considered a step towards ecological speciation and an important mechanism promoting diversification in phytophagous insects. Although the number of documented cases of HAD is increasing, these still represent only a small fraction of species and feeding guilds among phytophagous insects, and most reports are based on a single type of evidence. Here we employ a comprehensive approach to present behavioural, morphological, ecological and genetic evidence for the occurrence of HAD in the gall midge Dasineura folliculi (Diptera: Cecidomyiidae) on two sympatric species of goldenrods (Solidago rugosa and S. gigantea). Controlled experiments revealed assortative mating and strong oviposition fidelity for the natal-host species. Analysis of mitochondrial DNA showed an amount of genetic divergence between the two host-associated populations compatible with cryptic species rather than host races. Lower levels of within-host genetic divergence, gall development and natural-enemy attack in the S. gigantea population suggest this is the derived host.

Host-race formation: promoted by phenology, constrained by heritability.

Host-race formation is promoted by genetic trade-offs in the ability of herbivores to use alternate hosts, including trade-offs due to differential timing of host-plant availability. We examined the role of phenology in limiting host-plant use in the goldenrod gall fly (Eurosta solidaginis) by determining: (1) whether phenology limits alternate host use, leading to a trade-off that could cause divergent selection on Eurosta emergence time and (2) whether Eurosta has the genetic capacity to respond to such selection in the face of existing environmental variation. Experiments demonstrated that oviposition and gall induction on the alternate host, Solidago canadensis, were the highest on young plants, whereas the highest levels of gall induction on the normal host, Solidago gigantea, occurred on intermediate-age plants. These findings indicate a phenological trade-off for host-plant use that sets up the possibility of divergent selection on emergence time. Heritability, estimated by parent-offspring regression, indicated that host-race formation is impeded by the amount of genetic variation, relative to environmental, for emergence time.

Sequential radiation of unrelated organisms: the gall fly Eurosta solidaginis and the tumbling flower beetle Mordellistena convicta.

Host shifts and the formation of insect-host races are likely common processes in the speciation of herbivorous insects. The interactions of goldenrods Solidago (Compositae), the gall fly Eurosta solidaginis (Diptera: Tephritidae) and the beetle Mordellistena convicta (Coleoptera: Mordellidae) provide behavioural, ecological and genetic evidence of host races that may represent incipient species forming via sympatric speciation. We summarize evidence for Eurosta host races and show that M. convicta has radiated from goldenrod stems to Eurosta galls to form host-part races and, having exploited the galler's host shift, has begun to differentiate into host races within galls. Thus, host-race formation has occurred in two interacting, but unrelated organisms representing two trophic levels, resulting in 'sequential radiation' (escalation of biodiversity up the trophic system). Distributions of host races and their behavioural isolating mechanisms suggest sympatric differentiation. Such differentiation suggests host-race formation and subsequent speciation may be an important source of biodiversity.

The effects of drought on the Solidago altissima-Eurosta solidaginis-natural enemy complex: population dynamics, local extirpations, and measures of selection intensity on gall size.

Environmental catastrophes, such as severe drought, can reduce host-plant quality and/or abundance, which in turn decrease levels of herbivore populations. Such changes in herbivore populations affect populations of their natural enemies. As part of a long-term field experiment (1983-1991), galls of Eurosta solidaginis from 16 fields in central Pennsylvania were systematically collected from goldenrod ramets. Galls were dissected to compare the occurrence of E. solidaginis mortality caused by its natural enemies in 2 drought years (1988, 1991) with 5 pre-drought years (1983-1987) and 2 post-drought years (1989-1990). Gall diameters were significantly smaller in both drought years and early larval death significantly decreased E. solidaginis survivorship in the first drought year. Of the natural enemies, the parasitoid wasp Eurytoma gigantea caused significant selection for larger gall size in all pre-drought years, the 1991 drought, and both post-drought years, due to its differential attack of smaller galls. In spite of drought-induced small gall size in 1988, there was negligible selection on gall size by natural enemies. However, populations of E. solidaginis did suffer local extirpations at nine of the 16 fields during the first drought year and population recoveries of the gall inducer and natural enemies varied among fields in the post-drought years. As a consequence of reduced herbivore abundance in drought and post-drought years, some natural-enemy populations were absent. Drought therefore drastically reduced the abundance of E. solidaginis and natural enemies resulting in slow recoveries to pre-drought numbers.

The role of natural-enemy escape in a gallmaker host-plant shift.

The successful colonization of novel host-plant species by herbivorous insects may be facilitated by a reduction in natural-enemy attack on insect populations associated with the novel (derived) host plant. This is particularly true if natural enemies use host-plant or habitat cues in searching for their herbivore prey. In order to test whether the acquisition of enemy-free space could have influenced the host shift in the goldenrod ball gallmaker, Eurosta solidaginis, we estimated levels of natural-enemy attack in 25 host-race populations associated with Solidago altissima and S. gigantea (Compositae) spanning the zone of sympatry between S. altissima and S. gigantea host races in New England. Mortality due to attack by the parasitoid wasp Eurytoma obtusiventris was significantly higher for the ancestral than for the derived host race (30.5% versus 0.4%) across the transect, which is consistent with the enemy escape hypothesis. Contrary to this hypothesis, mordellid beetles caused significantly higher mortality on the derived than ancestral host race (17.1% versus 2.6%). Mortality by a second parasitoid wasp and birds showed no significant differences between the two host races. Overall, the derived host race had significantly higher survivorship across the transect (36.6% versus 20.8%). An analysis of survivorship and parasitoid mortality levels from sympatric sites in this study and previous studies showed a highly significant correlation between the levels of Eurytoma obtusiventris attack and the survivorship advantage of the derived host race. Observations of this parasitoid's searching behavior confirmed that it preferentially searches the ancestral host for fly larvae. Current patterns of host-race mortality and naturalenemy behavior and abundance are consistent with the facilitation of the host shift by escape from a specialist parasitoid.

Induction of a 58,000 dalton protein during goldenrod gall formation.

Despite the widespread occurrence of plant-gallmaker interactions, little is known about the actual mechanisms of gall formation. To further characterize this type of parasite-host interaction, the mechanism of gall formation in Solidago altissima, tall goldenrod, by the larva of the tephritid fly Eurosta solidaginis was studied. Proteins produced by galled and ungalled tissues were examined, and the hyperinduction of a 58 kilodalton protein was observed in galled tissues for the second and third week of gall growth. The presence of this protein suggests that a substance secreted by the larva may function as a trans-acting gene regulator.

Reproductive effort in clonal plants: constant allocation ratios among ramets?

Armstrong (1982, 1983) predicted that all ramets within a clone should have the same ratio of biomass allocation to sexual reproduction versus vegetative growth. He presented data (1984) that he interpreted as showing that Solidago altissima ramets in a clone do have the predicted constant allocation ratio. Reanalysis of his methods shows that this conclusion was an artifact of his analysis. A simulation using random numbers and Armstrong's analysis showed the same pattern as his data. Data from S. altissima ramets of a single clone grown in a greenhouse experiment, using a different analysis, illustrated that the allocation ratios within a clone can be highly variable.