Many microorganisms with specialized lifestyles have reduced genomes. This is best understood in beneficial bacterial symbioses, where partner fidelity facilitates loss of genes necessary for living independently. Specialized microbial pathogens may also exhibit gene loss relative to generalists. Here, we demonstrate that Escovopsis weberi, a fungal parasite of the crops of fungus-growing ants, has a reduced genome in terms of both size and gene content relative to closely related but less specialized fungi. Although primary metabolism genes have been retained, the E. weberi genome is depleted in carbohydrate active enzymes, which is consistent with reliance on a host with these functions. E. weberi has also lost genes considered necessary for sexual reproduction. Contrasting these losses, the genome encodes unique secondary metabolite biosynthesis clusters, some of which include genes that exhibit up-regulated expression during host attack. Thus, the specialized nature of the interaction between Escovopsis and ant agriculture is reflected in the parasite’s genome.

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Interactions between plants and herbivorous insects have been models for theories of specialization and co-evolution for over a century. Phytochemicals govern many aspects of these interactions and have fostered the evolution of adaptations by insects to tolerate or even specialize on plant defensive chemistry. While genomic approaches are providing new insights into the genes and mechanisms insect specialists employ to tolerate plant secondary metabolites, open questions remain about the evolution and conservation of insect counterdefences, how insects respond to the diversity defences mounted by their host plants, and the costs and benefits of resistance and tolerance to plant defences in natural ecological communities. Using a milkweed-specialist aphid (Aphis nerii) model, we test the effects of host plant species with increased toxicity, likely driven primarily by increased secondary metabolites, on aphid life history traits and whole-body gene expression. We show that more toxic plant species have a negative effect on aphid development and lifetime fecundity. When feeding on more toxic host plants with higher levels of secondary metabolites, aphids regulate a narrow, targeted set of genes, including those involved in canonical detoxification processes (e.g., cytochrome P450s, hydrolases, UDP-glucuronosyltransferases and ABC transporters). These results indicate that A. nerii marshal a variety of metabolic detoxification mechanisms to circumvent milkweed toxicity and facilitate host plant specialization, yet, despite these detoxification mechanisms, aphids experience reduced fitness when feeding on more toxic host plants. Disentangling how specialist insects respond to challenging host plants is a pivotal step in understanding the evolution of specialized diet breadths.

Studies of plant defenses and insect herbivores have been important in the development of our understanding of coevolution and specialization. Milkweed-herbivore systems have been a model for studying plant secondary chemistry defense evolution, insect adaptations to that chemistry, and coevolution between toxic plants and their herbivores for over a century. Yet, we are only beginning to unravel the multitude of adaptations required for insect specialization on milkweed plants. We review the empirical evidence for specialist insect adaptations toward milkweed toxins, coevolution between insects and milkweed plants, and canonical paradigms for sequestration and highlight the areas for further research. By comparing research performed with diverse milkweed insects, we discuss the need to comprehensively study adaptations and specialization in divergent insect taxa.

Parasites evolve within complex abiotic and biotic environments. Because of this, it is often challenging to ascertain how evolutionary and ecological processes together affect parasite specialization. Here, we use the fungus-growing ant system, which consists of ancient, likely coevolved, complex communities, to explore the ecological and evolutionary forces shaping host-parasite specificity. We use a comparative phylogenetic framework to determine whether patterns of specificity between the fungal parasite Escovopsis and its host fungi at fine phylogenetic scales reflect patterns of specificity at broader phylogenetic levels. In other words, we ask whether parasite specificity across broad host phylogenetic relationships is maintained by specificity toward more closely related hosts. We couple this exploration with manipulations of the community context within which host-parasite interactions are taking place to evaluate how community complexity alters parasite specificity. Regardless of host community complexity, parasites displayed a consistent pattern of specialization on native hosts, that is, those that they are found attacking in nature, with the potential for occasional switching to hosts distantly related to their native hosts. These results suggest that, even within a complex community context, pairwise host and parasite adaptation and coadaptation can be the primary drivers of the evolution and maintenance of parasite specificity.