Preference for C4 shade grasses increases hatchling performance in the butterfly, Bicyclus safitza

The Miocene radiation of C-4 grasses under high-temperature and low ambient CO2 levels occurred alongside the transformation of a largely forested landscape into savanna. This inevitably changed the host plant regime of herbivores, and the simultaneous diversification of many consumer lineages, including Bicyclus butterflies in Africa, suggests that the radiations of grasses and grazers may be evolutionary linked. We examined mechanisms for this plant-herbivore interaction with the grass-feeding Bicyclus safitza in South Africa. In a controlled environment, we tested oviposition preference and hatchling performance on local grasses with C-3 or C-4 photosynthetic pathways that grow either in open or shaded habitats. We predicted preference for C-3 plants due to a hypothesized lower processing cost and higher palatability to herbivores. In contrast, we found that females preferred C-4 shade grasses rather than either C-4 grasses from open habitats or C-3 grasses. The oviposition preference broadly followed hatchling performance, although hatchling survival was equally good on C-4 or C-3 shade grasses. This finding was explained by leaf toughness; shade grasses were softer than grasses from open habitats. Field monitoring revealed a preference of adults for shaded habitats, and stable isotope analysis of field-sampled individuals confirmed their preference for C-4 grasses as host plants. Our findings suggest that plant-herbivore interactions can influence the direction of selection in a grass-feeding butterfly. Based on this work, we postulate future research to test whether these interactions more generally contribute to radiations in herbivorous insects via expansions into new, unexploited ecological niches.