No abstract

Specialized trophic interactions in plant-herbivore-parasitoid food webs can spur "bottom-up" diversification if speciation in plants leads to host-shift driven divergence in insect herbivores, and if the effect then cascades up to the third trophic level.Conversely, parasitoids that search for victims on certain plant taxa may trigger "top-down" diversification by pushing herbivores into "enemy-free space" on novel hosts. We used phylogenetic regression methods to compare the relative importance of ecology versus phylogeny on associations between Heterarthrinae leafmining sawflies and their parasitoids. We found that: (1) the origin of leafmining led to escape from most parasitoids attacking external-feeding sawflies; (2) the current enemies mainly consist of generalists that are shared with other leafmining taxa, and of more specialized lineages that may have diversified by shifting among heterarthrines; and (3) parasitoid-leafminer associations are influenced more by the phylogeny of the miners' host plants than by relationships among miner species. Our results suggest that vertical diversifying forces have a significant-but not ubiquitous-role in speciation: many of the parasitoids have remained polyphagous despite niche diversification in the miners, and heterarthrine host shifts also seem to be strongly affected by host availability. K E Y W O R D S :Coevolution, enemy-free space, multitrophic networks, speciation, vertical diversification effects.

Genetic divergence and speciation in plant-feeding insects could be driven by contrasting selection pressures imposed by different plant species and taxa. While numerous examples of host-associated differentiation (HAD) have been found, the overall importance of HAD in insect diversification remains unclear, as few studies have investigated its frequency in relation to all speciation events. One promising way to infer the prevalence and repeatability of HAD is to estimate genetic differentiation in multiple insect taxa that use the same set of hosts. To this end, we measured and compared variation in mitochondrial COI and nuclear ITS2 sequences in population samples of leaf-galling Pontania and bud-galling Euura sawflies (Hymenoptera: Tenthredinidae) collected from six Salix species in two replicate locations in northern Fennoscandia. We found evidence of frequent HAD in both species complexes, as individuals from the same willow species tended to cluster together on both mitochondrial and nuclear phylogenetic trees. Although few fixed differences among the putative species were found, hierarchical AMOVAs showed that most of the genetic variation in the samples was explained by host species rather than by sampling location. Nevertheless, the levels of HAD measured across specific pairs of host species were not correlated in the two focal galler groups. Hence, our results support the hypothesis of HAD as a central force in herbivore speciation, but also indicate that evolutionary trajectories are only weakly repeatable even in temporally overlapping radiations of related insect taxa.

Studies on the determinants of plant-herbivore and herbivore-parasitoid associations provide important insights into the origin and maintenance of global and local species richness. If parasitoids are specialists on herbivore niches rather than on herbivore taxa, then alternating escape of herbivores into novel niches and delayed resource tracking by parasitoids could fuel diversification at both trophic levels. We used DNA barcoding to identify parasitoids that attack larvae of seven Pontania sawfly species that induce leaf galls on eight willow species growing in subarctic and arctic-alpine habitats in three geographic locations in northern Fennoscandia, and then applied distance- and model-based multivariate analyses and phylogenetic regression methods to evaluate the hierarchical importance of location, phylogeny and different galler niche dimensions on parasitoid host use. We found statistically significant variation in parasitoid communities across geographic locations and willow host species, but the differences were mainly quantitative due to extensive sharing of enemies among gallers within habitat types. By contrast, the divide between habitats defined two qualitatively different network compartments, because many common parasitoids exhibited strong habitat preference. Galler and parasitoid phylogenies did not explain associations, because distantly related arctic-alpine gallers were attacked by a species-poor enemy community dominated by two parasitoid species that most likely have independently tracked the gallers' evolutionary shifts into the novel habitat. Our results indicate that barcode- and phylogeny-based analyses of food webs that span forested vs. tundra or grassland environments could improve our understanding of vertical diversification effects in complex plant-herbivore-parasitoid networks.