The genetic architecture of a niche: variation and covariation in host use traits in the Colorado potato beetle

The genetic basis of host plant use by phytophagous insects can provide insight into the evolution of ecological niches, especially phenomena such as specialization and phylogenetic conservatism. We carried out a quantitative genetic analysis of multiple host use traits, estimated on five species of host plants, in the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). Mean values of all characters varied among host plants, providing evidence that adaptation to plants may require evolution of both behavioral (preference) and post-ingestive physiological (performance) characteristics. Significant additive genetic variation was detected for several characters on several hosts, but not in the capacity to use the two major hosts, a pattern that might be caused by directional selection. No negative genetic correlations across hosts were detected for any 'performance' traits, i.e. we found no evidence of trade-offs in fitness on different plants. Larval consumption was positively genetically correlated across host plants, suggesting that diet generalization might evolve as a distinct trait, rather than by independent evolution of feeding responses to each plant species, but several other traits did not show this pattern. We explored genetic correlations among traits expressed on a given plant species, in a first effort to shed light on the number of independent traits that may evolve in response to selection for host-plant utilization. Most traits were not correlated with each other, implying that adaptation to a novel potential host could be a complex, multidimensional 'character' that might constrain adaptation and contribute to the pronounced ecological specialization and the phylogenetic niche conservatism that characterize many clades of phytophagous insects.