Genetic Independence of Naturally Correlated Variation in Resistance to Endemic and Novel Pathogens

• Published in: Ecology letters Vol. 27; no. 10; pp. e14553 - n/a
• Main Authors: Hood, Michael E., Bruns, Emily L., Antonovics, Janis, Davis, Isabel, Launi, Michelle, Bulzoni, Sophia, Rothberg, Samantha E.
• Format: Journal Article
• Language: English
• Published: England Blackwell Publishing Ltd 01.10.2024
• Subjects: anther smut; disease emergence; Disease resistance; Disease Resistance - genetics; Genetic analysis; Genetic diversity; Genetic Variation; host shift; Microbotryum; nonhost resistance; Pathogens; Plant diseases; Plant Diseases - microbiology; Plant populations; Population genetics; Selection, Genetic; Silene; spillover; zoonosis; Microbotryum; spillover; anther smut; host shift; Silene; disease emergence; nonhost resistance; zoonosis
• ISSN: 1461-023X; 1461-0248; 1461-0248
• DOI: 10.1111/ele.14553

ABSTRACT The emergence of new diseases is an urgent concern, but hosts can also vary in resistance to pathogens that are novel to them, facilitating evolutionary rescue. However, little is known about the genetic source for polymorphic resistance to novel pathogens or its relationship to defences against endemic diseases. With anther‐smut disease from wild plant populations, we used selection experiments and genetic analyses to show that resistances to novel and endemic pathogens are genetically independent, despite being positively correlated in nature. Moreover, novel‐pathogen resistance presented a much simpler genetic basis and more rapid response to selection. We demonstrate that polymorphic resistance to a newly introduced disease is genetically determined and not an extension of defences against the related endemic pathogen, challenging the conventional view of nonhost resistance. The emergence of new diseases as an urgent concern, but the potential for wild hosts to evolve resistance to novel pathogens is a neglected issue. We find that populations of Silene vulgaris are polymorphic for resistance to a novel anther‐smut pathogen that correlates with resistance to a related endemic pathogen, but the genetic bases are independent and highly contrasting to expectations. The absence of pleiotropy suggests that broader ecological factors underlie the observed resistance correlation against multiple pathogens, which may be instrumental in determining the outcomes of newly introduced diseases.