A geographic mosaic of coevolution between Eurosta solidaginis (Fitch) and its host plant tall goldenrod Solidago altissima (L.).

A geographic mosaic of coevolution has produced local reciprocal adaptation in tall goldenrod, Solidago altissima (L.), and the goldenrod ball-gall fly, Eurosta solidaginis (Fitch 1855). The fly is selected to induce gall diameters that minimize mortality from natural enemies, and the plant is selected to limit gall growth that reduces plant fitness. We conducted a double reciprocal transplant experiment where S. altissima and E. solidaginis from three sites were grown in gardens at each site to partition the gall morphology variation into fly genotype, plant genotype, and the environment components. The host plant gall diameter induced by each E. solidaginis population was adapted to inhibit local natural enemies from ovipositing on or consuming enclosed larvae. Reciprocally, increasing the gall size induced by the local fly population increased the resistance of the local plant host population to gall growth. Differences among sites in natural enemies produced a mosaic of hotspots of coevolutionary arms races between flies selecting for greater gall diameter and plants for smaller diameters, and coldspots where there is no selection on plant or fly for a change in gall diameter. In contrast, the geographic variations of gall length and gall shape were not due to coevolutionary interactions.

Parallel environmental factors drive variation in insect density and plant resistance in the native and invaded ranges.

Geographic variation in the traits of a species is shaped by variation in abiotic conditions, biotic interactions, and evolutionary history of its interactions with other species. We studied the geographic variation in the density of the lace bug, Corythucha marmorata, and the resistance of tall goldenrod Solidago altissima to the lace bug herbivory in their native range in the United States and invaded range in Japan. We conducted field surveys and reciprocal transplant experiments to examine what abiotic and biotic factors influence variation in lace bug density, and what ecological and evolutionary factors predict the resistance of the host plant between and within the native and invaded ranges. Lace bug density was higher throughout the invaded range than in the native range, higher in populations with warmer climates, and negatively affected by foliage damage by other insects in both ranges. The higher lace bug density in warmer climates was explained by the shorter developmental time of the lace bugs at higher temperatures. The resistance of S. altissima to lace bugs was higher in populations with lace bugs compared to populations without lace bugs in both native and invaded ranges, indicating that the evolutionary history of the interaction with the lace bugs was responsible for the variation in S. altissima resistance in both ranges. The present study revealed that abiotic and biotic factors, including temperature and other herbivorous insects, can drive the geographic variation in lace bug density, which in turn selects for variation in plant resistance in both in the native and invaded ranges. We conclude that the novel combination of factors such as higher temperature and lower number of other herbivorous insects is responsible for the higher lace bug density in the invaded range than in the native range.

Plant genotypic diversity increases population size of a herbivorous insect.

It is critical to incorporate the process of population dynamics into community genetics studies to identify the mechanisms of the linkage between host plant genetics and associated communities. We studied the effects of plant genotypic diversity of tall goldenrod Solidago altissima on the population dynamics of the aphid Uroleucon nigrotuberculatum. We found genotypic variation in plant resistance to the aphid in our experiments. To determine the impact of plant genotypic diversity on aphid population dynamics, we compared aphid densities under conditions of three treatments: single-genotype plots, mixed-genotype plots and mixed-genotype-with-cages plots. In the latter treatment plants were individually caged to prevent natural enemy attack and aphid movement among plants. The synergistic effects of genotypes on population size were demonstrated by the greater aphid population size in the mixed-genotype treatment than expected from additive effects alone. Two non-exclusive hypotheses are proposed to explain this pattern. First, there is a source-sink relationship among plant genotypes: aphids move from plant genotypes where their reproduction is high to genotypes where their reproduction is low. Second, natural enemy mortality is reduced in mixed plots in a matrix of diverse plant genotypes.

Divergence of Eurosta solidaginis in response to host plant variation and natural enemies.

We tested the hypothesis that forest and prairie populations of the gall-inducing fly, Eurosta solidaginis, have diverged in response to variation in selection by its host plant Solidago altissima, and its natural enemies. A reciprocal cross infection design experiment demonstrated that fly populations from the prairie and forest biomes had higher survival on local biome plants compared to foreign biome host plants. Flies from each biome also had an oviposition preference for their local plants. Each fly population induced galls of the size and shape found in their local biome on host plants from both biomes indicating a genetic basis to the differences in gall morphology. Solidago altissima from the prairie and forest biomes retained significant morphological differences in the common garden indicating that they are genetically differentiated, possibly at the subspecies level. The populations are partially reproductively isolated as a result of a combination of prezygotic isolation due to host-associated assortative mating, and postzygotic isolation due to low hybrid survival. We conclude that E. solidaginis is undergoing diversifying selection to adapt to differences between prairie and forest habitats.

Geographic variation in the evolution and coevolution of a tritrophic interaction.

The geographic mosaic theory of coevolution predicts that geographic variation in species interactions will lead to differing selective pressures on interacting species, producing geographic variation in the traits of interacting species (Thompson 2005). We supported this hypothesis in a study of the geographic variation in the interactions among Eurosta solidaginis and its natural enemies. Eurosta solidaginis is a fly (Diptera: Tephritidae) that induces galls on subspecies of tall goldenrod, Solidago altissima altissima and S. a. gilvocanescens. We measured selection on E. solidaginis gall size and shape in the prairie and forest biomes in Minnesota and North Dakota over an 11-year period. Galls were larger and more spherical in the prairie than in the forest. We supported the hypothesis that the divergence in gall morphology in the two biomes is due to different selection regimes exerted by natural enemies of E. solidaginis. Each natural enemy exerted similar selection on gall diameter in both biomes, but differences in the frequency of natural enemy attack created strong differences in overall selection between the prairie and forest. Bird predation increased with gall diameter, creating selection for smaller-diameter galls. A parasitic wasp, Eurytoma gigantea, and Mordellistena convicta, an inquiline beetle, both caused higher E. solidaginis mortality in smaller galls, exerting selection for increased gall diameter. In the forest there was stabilizing selection on gall diameter due to a combination of bird predation on larvae in large galls, and M. convicta- and E. gigantea-induced mortality on larvae in small galls. In the prairie there was directional selection for larger galls due to M. convicta and E. gigantea mortality on larvae in small galls. Mordellistena convicta-induced mortality was consistently higher in the prairie than in the forest, whereas there was no significant difference in E. gigantea-induced mortality between biomes. Bird predation was nonexistent in the prairie so the selection against large galls found in the forest was absent. We supported the hypothesis that natural enemies of E. solidaginis exerted selection for spherical galls in both biomes. In the prairie M. convicta exerts stabilizing selection to maintain spherical galls. In the forest there was directional selection for more spherical galls. Eurytoma gigantea exerted selection on gall shape in the forest in a complex manner that varied among years. We also supported the hypothesis that E. gigantea is coevolving with E. solidaginis. The parasitoid had significantly longer ovipositors in the prairie than in the forest, indicating the possibility that it has evolved in response to selection to reach larvae in the larger-diameter prairie galls.