Transcriptomic Landscape Reveals Immunity Related Trade-Offs in an Invertebrate-Fungal Host–Parasite System

Abstract

Host–parasite interactions represent an evolutionary arms race, with parasites evolving strategies to exploit host resources, and hosts deploying mechanisms to resist or tolerate infection. Unlike vertebrates, which possess a sophisticated immune system, invertebrates rely entirely on innate immunity to combat pathogens. Yet, the molecular underpinnings and life-history consequences of immune activation remain little understood in non-insect invertebrates. Here, we combine life-history trait analysis with transcriptomics to investigate immune responses in an aquatic invertebrate exposed to a natural yeast parasite. By comparing infected, exposed-uninfected, and unexposed individuals, we identified candidate genes potentially involved in haemocyte recruitment and the reinforcement of the gut epithelium. These patterns highlight candidate mechanisms that may contribute to resistance following pathogen exposure. Exposed-uninfected individuals also showed delayed reproductive maturation, though lifetime reproductive output was ultimately maintained. Therefore, this suggests that successful exposure and immunity changes may be associated with a transient shift in reproductive allocation rather than a persistent reduction in reproductive output. In contrast, infected hosts exhibited stronger changes in metabolic and protein biosynthesis processes, consistent with a resource depletion hypothesis. These metabolic shifts align with reduced investment in reproduction, as infection appears to affect the number of offspring produced in the first brood. Our findings provide novel insights into the molecular and life-history responses associated with pathogen exposure and established infection and suggest candidate mechanisms through which host responses may shape life-history strategies in non-insect invertebrates, with broad implications for understanding host–parasite coevolution.