Widespread sex-biased gene expression reflects female-biased longevity in a species with environmental sex determination

Abstract

Sexes frequently differ in life history traits including body size, lifespan, and age at sexual maturity. Aging, the progressive decline in physiological function and cellular resilience over time, is a central process contributing to sex-specific life histories, yet the mechanisms driving sex differences in aging remain largely unresolved. Long-term mark-recapture efforts revealed a striking pattern of female-biased longevity in the painted turtle (Chrysemys picta), a species with temperature-dependent sex determination. As a result, this species provides a compelling system to examine the mechanisms of sex-specific aging in the absence of sex chromosomes. Here, we characterize sex- and age-associated patterns in the blood transcriptomes of wild painted turtles (n = 93). We identified widespread gene expression differences between females and males (2,347 genes; 13.4% of all filtered genes). In contrast, only six genes showed significant linear relationships with continuous age in both sexes. We also employed a machine learning approach which identified distinct sets of genes for which expression was predictive of age in each sex. Age-related gene expression patterns highlight both conserved molecular pathways with known roles in aging as well as novel gene targets. These findings suggest sex-specific molecular processes underlie sex-biased demographic aging and raise questions regarding the environmental and developmental drivers of sex-biased gene expression.