Improving Natural Enemy Selection in Biological Control through Greater Attention to Chemical Ecology and Host-Associated Differentiation of Target Arthropod Pests

SIMPLE SUMMARY: Some species of insect herbivores can feed on a wide variety of plant species. Over evolutionary time, insect herbivores can associate preferentially with different host-plant species, which frequently leads to genetic divergence between populations of an herbivore species. This phenomenon, referred to as host-associated differentiation (HAD), not only affects insect herbivores, but can also impact their associated natural enemies, particularly predatory or parasitic insects, which are responsible for biological control in agroecosystems. Although the mechanisms underlying HAD in populations of herbivores and associated natural enemies remain underexplored, we argue that the chemical communication between plants, herbivores, and natural enemies likely plays a major role. Chemical cues emitted by plants and insect herbivores influence natural enemy foraging behavior, and divergent chemical cues can lead to natural enemy HAD, ultimately shaping biological control. In this synthesis paper, we explore how the chemical ecology of HAD could influence classical, conservation, and augmentative biological control, and propose research agendas to further biological control efficacy through natural enemy selection. ABSTRACT: Host-associated differentiation (HAD) refers to cases in which genetically distinct populations of a species (e.g., herbivores or natural enemies) preferentially reproduce or feed on different host species. In agroecosystems, HAD often results in unique strains or biotypes of pest species, each attacking different species of crops. However, HAD is not restricted to pest populations, and may cascade to the third trophic level, affecting host selection by natural enemies, and ultimately leading to HAD within natural enemy species. Natural enemy HAD may affect the outcomes of biological control efforts, whether classical, conservation, or augmentative. Here, we explore the potential effects of pest and natural enemy HAD on biological control in agroecosystems, with emphases on current knowledge gaps and implications of HAD for selection of biological control agents. Additionally, given the importance of semiochemicals in mediating interactions between trophic levels, we emphasize the role of chemical ecology in interactions between pests and natural enemies, and suggest areas of consideration for biological control. Overall, we aim to jump-start a conversation concerning the relevance of HAD in biological control by reviewing currently available information on natural enemy HAD, identifying challenges to incorporating HAD considerations into biological control efforts, and proposing future research directions on natural enemy selection and HAD.