Larval and adult experience and ecotype affect oviposition behavior in a niche-expanding butterfly

Local adaptation, early-developmental and behavioral plasticity have all been suggested to be underlying mechanisms of behavioral variation. They allow organisms to cope with resource heterogeneity in time and space. However, the relative contribution of each of these drivers on niche-expansion success is still unclear. We addressed this issue by studying oviposition behavior in a butterfly (Pararge aegeria) that used to be confined to forest, but recently colonized anthropogenic areas too. We caught females of either forest or agricultural ecotype and allowed their larval offspring to experience early-habitat cues in either open field or woodland conditions. For 110 females of this transplant experiment, we monitored all oviposition-related behaviors (i.e., site selection, searching, motivation, learning) using repeated trials in outdoor flight cages with naturally occurring host grasses. We observed changes in oviposition site preference, with increasing preference for semi-shaded host grass (by vegetation or vertical structures) over consecutive egg-lays. Motivation to oviposit was most affected by larval experience (in interaction with cage environment). We also show evidence for ecotypic differentiation with the agricultural ecotype showing reduced search effort during the first trial compared to the forest ecotype. We argue that females of agricultural landscapes with fragmented resource distributions adopt a more risk-aversive oviposition strategy. Our detailed behavioral tracking under ecologically relevant conditions, stresses the importance of considering different types of behavioral plasticity to unravel a species' success during niche expansion. Local adaptation and behavioral plasticity may both facilitate rapid niche expansion. We studied a butterfly species that expanded its habitat use from forest to anthropogenic environments. Using a larval, reciprocal transplant experiment and detailed oviposition tracking in outdoor flight cages, we show effects of ecotype, larval and adult experience. We argue for combined effects of local adaptation, natal habitat preference induction and short-term memory learning on the multi-featured behavioral repertoire during oviposition.