Sexually antagonistic selection, X-chromosome relatedness and the evolution of menopause in killer whales

The human menopause is hypothesized to be an adaptive trait that allows post-reproductive females to invest in, and avoid reproductive conflict with, their existing offspring and grand-offspring, thereby increasing their survival. Thus, the sacrifice of an early cessation of reproduction can result in increased inclusive fitness. However, the genetic basis of menopause remains largely unknown. Given that a mid-life menopause is a rare trait in terrestrial social species, there is a need to consider alternative taxa to move beyond a single datapoint to test theoretical frameworks upon. One aquatic taxonomic group, toothed whales, comprises five matrilineal species with menopause, thereby providing a crucial comparative system for understanding the evolution of menopause. The kinship dynamics in killer whale Orcinus orca societies, maximize the inclusive fitness of post-reproductive females when they invest in their son's reproductive success. Specifically, inclusive fitness is maximized at the X-chromosome (over the autosomes) through a post-reproductive female's son siring daughters. This raises the question of how selection favours a female trait that primarily benefits male offspring? Due to its inheritance pattern and ploidy, the X-chromosome is a candidate target for sexual antagonistic selection, which could act on the female-specific traits of increased lifespan and reproductive cessation. We therefore propose that the X-chromosome is a promising marker to explore the genetic underpinning of menopause in matrilineal whale species and could provide a key comparison (and contrast) to the genetic basis of menopause in humans. Lastly, we expand these ideas to autosomal regions with female biased recombination.