Insect hosts are nutritional landscapes navigated by fungal pathogens

Abstract

Nutrition can mediate host–pathogen interactions indirectly when specific deficiencies (e.g., iron or glutamine) constrain host immune performance. Nutrition can also directly govern these interactions as invading pathogens colonize finite landscapes of nutritionally variable host tissues that must be optimally foraged during pathogen development. We first used a conceptual framework of nutritional niches to show that insect-pathogenic Metarhizium fungi navigate host landscapes where different tissues vary widely in (protein [P] and carbohydrates [C]). We next tested whether host-specific Metarhizium species have narrower fundamental nutritional niches (FNNs) than host-generalists by measuring pathogen performance across an in vitro nutritional landscape simulating a within-host foraging environment. We then tested how developing pathogens navigate nutritional landscapes by developing a liquid-media approach to track pathogen intake of P and C over time. Host-specificity did not govern FNN dimensions, as the three tested Metarhizium species: (1) grew maximally across C treatments assuming P was present above a lower threshold, and (2) similarly initiated dispersal behaviors and sporulated when either C or P became depleted. However, specialist and generalist pathogens navigated nutritional landscapes differently. The host specialist (M. acridum) first prioritized C intake, but generalists (M. anisopliae, M. robertsii) prioritized P and C according to their availability. The numbers of known hosts may be insufficient to delimit pathogens as specialists or generalists as diverse hosts do not necessarily comprise diverse nutritional landscapes. Instead, the immune responses of hosts and nutritional niche breadth of pathogens are likely co-equal evolutionary drivers of host specificity.