Modern evidence of non-genetic inheritance mechanisms that operate alongside and in conjunction with genetic inheritance has revolutionized our understanding of how variation is transmitted across generations. Maternal effects have long been recognised as having important non-genetic influences on offspring phenotype. In contrast, males are often considered to contribute ‘nothing but sperm’ to reproduction. A sperm’s job is to deliver DNA to an egg, and DNA is not influenced by the environment. Hence, it was thought that the paternal environment could not influence offspring traits. Using two very different study systems – sea squirts and neriid flies – I have empirically demonstrated that plasticity in sperm and semen quality can influence offspring growth and survival, even in species that provide ‘nothing but sperm’.
Observed patterns of inheritance suggest that different mechanisms are driving non-genetic paternal effects in each system. Sea squirts reproduce by releasing both eggs and sperm into the ocean where fertilization occurs, making them a very tractable system to examine links between sperm plasticity and offspring phenotype. I found that males in high density environments make more competitive sperm (increasing fertilization success) at a cost to successful offspring development. However, post-settlement, offspring survive better when their environment matches their fathers, suggesting that males may be able to prepare their offspring for future environmental challenges. Neriid flies mate like the majority of land animals, but fly eggs are not fertilized until immediately before they are laid. This allowed me to decouple exposure to seminal fluid from fertilization, showing that the diet of a mating partner who does not sire offspring can influence the size of future offspring sired by another male. Not only does this remarkable effect change the way we view inheritance, it also tells us that non-sperm components of the seminal fluid can mediate non-genetic paternal effects.