We report evidence of adaptive evolution in juvenile development time on a decadal timescale for the cinnabar moth Tyria jacobaeae (Lepidoptera: Arctiidae) colonizing new habitats and hosts from the Willamette Valley to the Coast Range and Cascades Mountains in Oregon. Four lines of evidence reveal shorter egg to pupa juvenile development times evolved in the mountains, where cooler temperatures shorten the growing season: (i) field observations showed that the mountain populations have shorter phenological development; (ii) a common garden experiment revealed genetic determination of phenotypic differences in juvenile development time between Willamette Valley and mountain populations correlated with the growing season; (iii) a laboratory experiment rearing offspring from parental crosses within and between Willamette Valley and Cascades populations demonstrated polygenic inheritance, high heritability, and genetic determination of phenotypic differences in development times; and (iv) statistical tests that exclude random processes (founder effect, genetic drift) in favor of natural selection as explanations for observed differences in phenology. These results support the hypothesis that rapid adaptation to the cooler mountain climate occurred in populations established from populations in the warmer valley climate. Our findings should motivate regulators to require evaluation of evolutionary potential of candidate biological control organisms prior to release.

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The cinnabar moth, Tyria jacobaeae (L.) (Lepidoptera: Arctiidae), is an icon in population ecology and biological control that has recently lost its shine based on evidence that (a) it is less effective than alternatives (such as the ragwort flea beetle Longitarsus jacobaeae (Waterhouse) Coleoptera: Chrysomelidae) for controlling ragwort, Senecio jacobaea L. (Asteraceae), (b) it eats (harms) non-target plant species (including arrowleaf ragwort, Senecio triangularis Hook. (Asteraceae), a native North American wildflower, and potentially harms the animals that depend on these native plant species and (3) it carries a disease (caused by a host-specific microsporidian Nosema tyriae). We used a life table response experiment (LTRE) combining a factorial experiment and a matrix model to estimate the independent and interacting effects of Old World and New World host plant species (first trophic level) and the entomopathogen (third trophic level) on the life cycle and population growth of the cinnabar moth (second trophic level). Host shifts are expected if herbivore fitness is higher on novel compared with conventional host plants, perhaps because the advantage of reduced effectiveness of herbivore natural enemies outweighs the disadvantage of herbivore malnutrition associated with novel host plants. Contrary to this hypothesis, we found the population growth rate of the cinnabar moth is sharply reduced on novel compared with conventional host plants by interacting effects of disease and malnutrition. Paradoxically, a pathogen of the cinnabar moth may enhance weed biological control by providing insurance against host shifts.

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