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

Abstract

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.

Phylogenetic, Spatial, and Species‐Trait Patterns across Environmental Gradients: the Case of Hydropsyche (Trichoptera) along the Loire River

“…Obviously, taxa with marine ancestors that evolve along rivers starting from river mouths should primarily evolve into the upstream direction (VANNOTE et al, 1980;PENNAK, 1985). In any case, however, the steps should have been relatively short because the environmental gradi-ents along running waters are so constraining that it requires gradual adaptation of multiple systems to evolve across these gradients (similarly to adaptations of phytophagous insects to new host plants; FORISTER et al, 2007).…”

“…If lotic insect speciation occurred stepwise through river networks, we would expect stepwise adaptations of species traits to the steep environmental gradients prevailing along rivers. Typically, phylogenetic niche conservatism limits niche divergence if speciation would require a multidimensional adaptation to a complex situation (PRINZING et al, 2001;FORISTER et al, 2007;VAMOSI and VAMOSI, 2007). Consequently, an insect clade that speciated through river networks should exhibit similar gradients in phylogeny and species traits that represented adaptations to the environmental changes prevailing along rivers (our fourth hypothesis).…”

Hybridization leads to host-use divergence in a polyphagous butterfly sibling species pair

“…Significant genetic correlations would indicate that the traits conferring the abilities to use particular hosts may not be independent. In particular, negative correlations may indicate potential trade-offs and positive correlations might facilitate the evolution of generalization (e.g., Forister et al 2007). We first tested whether there were significant differences in the performance of late flight families on one host relative to their performance on another host (i.e., a significant difference between the norms of reaction of late flight families).…”

A genetic perspective on insect climate specialists

“…For host use, strain comparisons in the Colorado potato beetle, Leptinotarsa decemlineata Say (Coleoptera: Chrysomelidae), suggest that changes in behavioural and performance traits are uncorrelated, which tends to support the notion that multiple traits evolving independently might make it difficult for host shifts to occur (Forister et al 2007). For high temperature resistance, selection experiments and strain comparisons with D. melanogaster suggest that different components of heat response are uncorrelated (Hoffmann et al 2003b), and this might make it more difficult for populations to adapt to increasing temperatures.…”