Butterflies embrace maladaptation and raise fitness in colonizing novel host.

We illustrate an evolutionary host shift driven by increased fitness on a novel host, despite maladaptation to it in six separate host-adaptive traits. Here, local adaptation is defined as possession of traits that provide advantage in specific environmental contexts; thus individuals can have higher fitness in benign environments to which they are maladapted than in demanding environments to which they are well adapted. A population of the butterfly adapted to a long-lived, chemically well-defended host, had traditionally been under natural selection to avoid the ephemeral, less-defended . The lifespan of was so short that it senesced before larvae entered diapause. After logging killed in clear-cut patches and controlled burning simultaneously extended lifespan, insect fitness on in clearings suddenly became higher than on in adjacent unlogged patches. was rapidly colonized and preference for it evolved, but insects feeding on it retained adaptations to in alighting bias, two aspects of postalighting oviposition preference, dispersal bias, geotaxis, and clutch size, all acting as maladaptations to . Nonetheless, populations boomed on in clearings, creating sources that fed pseudosinks in unlogged patches where was still used. After c. 20 years, butterfly populations in clearings disappeared and the metapopulation reverted to -feeding. Here we show, via experimental manipulation of oviposition by local -adapted and imported -adapted butterflies, that the highest survival at that time would have been from eggs laid in clearings by butterflies adapted to . Second highest were locals on . In third place would have been locals on in clearings, because local females maladaptively preferred senescent plants. had been colonized despite maladaptation and, after successional changes, abandoned because of it. However, the abandoned could still have provided the highest fitness, given appropriate adaptation. The butterflies had tumbled down an adaptive peak.