Frontiers in immunology · 2026
Changes in gene regulation are associated with the evolution of resistance to a novel parasite.
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Fuess Lauren E, Hund Amanda K, Kenney Mariah L, Maciejewski Meghan F, Marini Joseph M, Bolnick Daniel I
Аннотация
INTRODUCTION: Host-parasite interactions are ubiquitous and are important drivers of host diversification and evolution. In particular, host immune systems are frequent targets of parasite-driven selection. The resulting rapid evolution of immune genes is usually framed as an ongoing 'arms race' between a co-evolving pair of host and parasite species. However, immune evolution may often be driven by the acquisition of a new and unfamiliar parasite. For instance, when marine populations of threespine stickleback (Gasterosteus aculeatus) colonized freshwater lakes approximately 12,000 years ago, they encountered the freshwater-restricted cestode Schistocephalus solidus and evolved resistance.
METHODS: We compared the transcriptomic responses of lab-reared sticklebacks from three populations of stickleback with varying cestode susceptibilities when exposed to several immune stimuli (alum, cestode protein, or a control injection).
RESULTS: The resulting changes in expression reveal strong evidence of shared and population-specific responses during the evolution of defense against a new parasite. Our investigation highlights the roles of several key immunological processes in underlying a general physiological response to tissue damage (fibrosis) and the importance of regulating fibrosis as a necessary step for its co-option into defense against S. solidus tapeworms. Furthermore, we highlighted changes in the expression of fibrosis-associated genes, which facilitate faster and more targeted deployment of this defense mechanism against parasites. Fish from the most fibrosis-prone population exhibited constitutively higher expression of fibrosis-associated genes and stronger downregulation of these genes after an initial stimulus from injected cestode proteins.
CONCLUSION: Our results provide strong evidence that changes in gene regulation and increased negative feedback to mitigate immunopathology are essential steps in the evolutionary co-option of an existing pathway to defend against a new parasite infection.
METHODS: We compared the transcriptomic responses of lab-reared sticklebacks from three populations of stickleback with varying cestode susceptibilities when exposed to several immune stimuli (alum, cestode protein, or a control injection).
RESULTS: The resulting changes in expression reveal strong evidence of shared and population-specific responses during the evolution of defense against a new parasite. Our investigation highlights the roles of several key immunological processes in underlying a general physiological response to tissue damage (fibrosis) and the importance of regulating fibrosis as a necessary step for its co-option into defense against S. solidus tapeworms. Furthermore, we highlighted changes in the expression of fibrosis-associated genes, which facilitate faster and more targeted deployment of this defense mechanism against parasites. Fish from the most fibrosis-prone population exhibited constitutively higher expression of fibrosis-associated genes and stronger downregulation of these genes after an initial stimulus from injected cestode proteins.
CONCLUSION: Our results provide strong evidence that changes in gene regulation and increased negative feedback to mitigate immunopathology are essential steps in the evolutionary co-option of an existing pathway to defend against a new parasite infection.