MHC diversity confers transgenerational fitness advantage in wild dolphins

Abstract Darwin ascribed fitness to individuals with a “better chance of surviving and propagating their kind”¹. Subsequently, the search for the genetic basis of fitness focused on traits of the generation that had been genotyped. However, there is only scant, indirect evidence for genetic variation conferring transgenerational fitness effects to subsequent generations²⁻⁵. Specifically, there is no direct evidence for a link between parental genetic variation and offspring fitness in long-lived, natural populations. Here we show transgenerational fitness effects mediated by adaptive genetic variation of the major histocompatibility complex (MHC) in a natural population of bottlenose dolphins. Our study, spanning nearly four decades of research (1984­2022), revealed that offspring of MHC-heterozygous mothers were twice as likely to survive. The mother’s age and MHC-heterozygosity were strong predictors of offspring viability. In contrast, we found no association between neutral genetic diversity and fitness. Interestingly, MHC-heterozygous females were less sociable, perhaps an indirect effect of them being more successful mothers that prioritize offspring investment over social bonds—in contrast to other social mammals that rely on female relationships to mediate fitness⁶. To our knowledge, this is the first study that offers empirical evidence for MHC diversity conferring a fitness advantage across generations. This is in line with theorized, but rarely tested expectations for MHC-dependent mate choice⁴. Our study also underscores the crucial role of long-term studies⁷ in revealing the genetic basis of fitness in long-lived, natural populations.