No one is overly surprised when kids look like their fathers. Children contain genes from both parents so naturally they look and act a bit like each one. But what if your offspring look less like your actual mate than your former one? Is it a scandal? Maybe, but not necessarily. In an elegant new paper in Ecology Letters, Angela Crean and her Australian colleagues show that this unexpected resemblance may just be due to ‘telegony’.
Telegony is the long-ago discredited idea that males can influence not just their own genetic offspring, but also future offspring produced by the same female sired by different males. Most problematically, the idea lacked evidence. Equally, it lacked a mechanism and clashed fundamentally with the modern understanding of mendelian inheritance. How, after all, could a father influence offspring to which it contributed no genes?
As shown by Crean and her colleagues, the answer – at least for a group of Australian flies – turns out to be less complicated than you might think. Like many insects, young female neriid flies produce immature eggs that take several weeks to fully develop. Although males that mate with females during this interval sire no offspring, the research team hypothesized that they could still influence her future offspring. Importantly, males don't only transfer sperm during mating. They also transfer seminal fluid containing a diverse cocktail of proteins that have wide ranging effects on female physiology – and potentially on their immature eggs.
To test this idea, the team first mated immature female flies with two types of males. The first were well fed and in prime condition while the second were food deprived. In previous studies, the group found that big males tended to give rise to big offspring while food-deprived males tended to produce runts. Here, because the eggs were immature, neither treatment group was expected to sire any offspring at all. However, via their semen, these males could still modify the environment in which the eggs completed development.
Once the females had matured, they were mated for a second time with males of the two treatment groups and allowed to lay their fertilised eggs. Strikingly, the team found that the size of the offspring of these twice-mated females was better predicted by the size of their first mate than by the size of the actual genetic father. If the first mate was big, so too were the offspring, even if the second mate was a runt. And this, in a nutshell, is telegony.
Non-genetic factors, especially the maternal environment have long been recognized as key determinants of offspring phenotype. If mom drinks, smokes or has a poor diet, this can lead to syndromes in offspring that reflect the conditions they experienced in utero. By contrast, paternal influences have been largely ignored because dads – absent parental care – are just sperm machines, right? The results of this study add to the mounting evidence that this assumption is plainly false and the implications of this are far-reaching. Could loser males benefit from the semen of high-quality males, or high-quality males suffer from the miserable semen of losers? Can females distinguish high genetic quality males from those whose telegonic ‘fathers’ were high quality? More generally, what does ‘quality’ even mean if non-genetic factors can so easily decouple phenotype and genotype? Answering these questions, as well as clarifying the generality of telegony, remain fascinating research areas for the future.
