Interacting effects of sex and age on immune responses in a polygynous bat with male-biased mortality

Abstract Bats have attracted considerable interest for their extraordinary longevity and ability to withstand infection by a range of pathogens without major harm. Yet, little is known about the relationship between these two characteristics, or the extent to which they vary between individuals of the same species. We investigated sources of immune variation in wild greater spear-nosed bats, Phyllostomus hastatus, via transcriptome sequencing of blood samples before and after ex vivo exposure to lipopolysaccharide, a membrane component of gram-negative bacteria. This species exhibits an extreme harem-polygynous mating system and strongly male-biased mortality, offering the valuable opportunity to explore sources of individual variation in immunity and its relation to ageing. We assessed immune variation across both sexes, males of contrasting social status, and the full range of ages in each sex. We observe striking immune variation associated with sex and age, with males and older bats mounting stronger inflammatory responses. These two factors interacted significantly, revealing male-biased slopes of age-related variation in immunity, the magnitude of which is consistent with male-biased ageing, supporting the predicted association between immunity and ageing. We did not observe substantial differences in immune responses between males of harem-controlling or subordinate bachelor status. This contrasts with prior research, particularly in primates, potentially raising questions about the taxonomic generality of socially mediated immune differences, which have attracted much attention. Our findings support recent calls for a nuanced approach to understanding immune adaptations and extended longevity in bats, informed by individual and species-level differences in ecology, resource allocation, and selection. These widely overlooked factors offer valuable insights into sources of immune variation and connections to other traits, such as differences in mortality and age-related deterioration. Competing Interest Statement The authors have declared no competing interest. Footnotes Title changed. All figures updated for clarity. Analysis updated throughout with small changes to results due to decisions made in analysis (e.g., removal of genes included in ribosomal/globin probe pools). Additional detail added to Abstract and Methods sections. Introduction and Discussion sections rewritten for conciseness.