Because mothers can influence their offspring in a number of ways, from copulation to birth, while fathers have control over sperm only, it has long been assumed mothers are more important. In mammals, it is also believed that offspring sex ratios can only be determined by the mother, since fathers have always been thought to inseminate an equal proportion of X and Y sperm, having a random effect on offspring sex that they could not shift from equality, or 50:50.
Not so, according to a new paper in Proceedings of the Royal Society B. Using a wild rodent model – the white-footed mouse – in lab conditions, the authors found that there was a relationship between a father's "genetic quality" and the proportion of sons and daughters he has. They then showed that this relationship is mediated by a trait that is exclusive to the father: the size of the nuclei in their sperm, which reflects the proportion of X to Y sperm.
Fathers with higher genetic quality produce sperm with smaller head nuclei – a higher proportion of Y sperm – and go on to produce more sons than daughters. "The implications are important, as we now have the proof that fathers matter independently of any maternal effects. Scientists can now improve their predictive models of sex ratios at birth, including not only mothers but also fathers," according to Dr Aurelio Malo of Oxford University's Department of Zoology.
Relationship between a father's mean sperm nucleus area (or nucleus length; inset graph) and its offspring sex ratio. Each data point reflects the mean calculated using a minimum of 200 sperm per male. Two outlier data points for sperm nucleus area were removed (2.85 s.d. and 3.12 s.d. away from the mean sperm nucleus area). n = 38. DOI: 10.1098/rspb.2017.1159
They have an idea as to why it's in the father's evolutionary interests to alter the probability of having sons or daughters, the same way it is for mothers (physical costs of gestation are obviously higher for the mother, so it's in her own interests from an evolutionary point of view to invest her resources wisely in terms of the sex, size and quality of her offspring.) According to Malo, one plausible reason is that males of lower genetic quality minimize the cost of having sons, which are more susceptible to the negative effects of inbreeding on fertility, by shifting the sex ratio to daughters, which are more resilient to these negative effects of inbreeding.
"Predicting sex ratios has great interest for humans, as well as bioethical implications. In domestic species, such as livestock and pets, the ability to manipulate sex ratios has important economic implications. In endangered species, skewed population sex ratios can push species to the brink of extinction, so breeding programs could pair males and females according to individual attributes that help achieve the rarer sex at birth," Malo says.
By showing that fathers can adjust sex ratios by varying sperm types, rather inseminating the same proportion of X and Y sperm generated at meiosis, the authors hope to advance research in paternal effects on sex ratios. For example, do mothers and fathers have the same or opposing sex allocation interests? Does this vary across species and contexts?
'In a nutshell, we now know that dads, as well as mums, can alter the sex of their offspring, and that the ability to do so might have evolved through natural selection.'
Citation: Aurelio F. Malo, Felipe Martinez-Pastor, Francisco Garcia-Gonzalez, Julián Garde, Jonathan D. Ballou, Robert C. Lacy, 'A father effect explains sex-ratio bias', 30 August 2017. DOI: 10.1098/rspb.2017.1159