Daughter or son, which sex to produce?

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Schindler, S., Gaillard, J., Grüning, A., Neuhaus, P., Traill, L., Tuljapurkar, S., & Coulson, T. (2015). Sex‐specific demography and generalization of the Trivers–Willard theory Nature, 526 (7572), 249-252 DOI: 10.1038/nature14968

The right offspring sex can increase the number of grandchildren. Theory predicts which offspring sex is optimal depending on the mother’s condition, but mothers in natural populations do not behave according to theoretical predictions. We explain the reason for the mismatch and provide more accurate predictions.

Female bighorn sheep with her young.

Female bighorn sheep with her young. (c) Peter Neuhaus

Suppose you are a ewe (female sheep) and suppose you could choose the sex of your one offspring. A son in good condition might become a harem leader and sire several grand-lambs, while a son in poor condition would be unable to compete with harem leaders and would not sire any offspring. A daughter produces approximately one fawn each year independent of her condition, so which sex would you produce?

It depends on the ewe’s condition: if she is in good condition she is likely to produce a good-condition fawn and that should be a male. If she is in poor condition her fawn is likely to be in poor condition too and she should produce a daughter, because the daughter will have low but nearly guaranteed reproductive success.

Mothers that can choose the offspring sex have a higher number of descendants and the ability to choose offspring sex is expected to spread in the population. This is the core of the famous Trivers-Willard theory. Trivers and Willard proposed the theory in the 70’s and since then it has been continuously tested in natural populations**. However, the empirical results do not match theoretical predictions. In some populations, researcher found a correlation between mother’s condition and offspring sex, in others not. Sometimes the correlation was reversed, that is good-conditioned mothers produced more daughters than son. Some data in some years supported the theory, in other years not. In sum, despite the elegance of the theory, support for it has been limited. Why?

Explanations fall into three broad categories: first, a female might be unable to determine the sex of her offspring, second, data quality is insufficient, and third, empirical tests were performed on species which do not fulfil the assumptions of the theory. The four assumptions of Trivers-Willard theory are that (1) maternal condition determines offspring condition, (2) offspring condition at weaning persists into adulthood, (3) good-condition males produce more offspring than poor-condition ones, and (4) there is greater variation in lifetime reproductive success among males than females.

These assumptions are generally fulfilled in polygynous species where males mate with multiple females and grow larger than females. However, male mortality in these species is typically higher than for females because they lead a more risk-prone life which involves more fighting, higher maintenance costs, and later age at reproduction, as they need longer to reach bigger body size. These differences between females and males were not incorporated in the theory but are likely to matter for the optimal offspring sex strategy. Therefore, we developed a model that accounts for sex-differences and analysed optimal sex-allocation.

There are two major results from the model. The first result is that the optimal sex-allocation strategy for mothers is very sensitive to differences in mortality rates, growth rates, fertility rates, and mating success. That means, if environmental conditions change from one year to the next, the optimal choice of offspring sex might well be different each year. The consequence for empirical tests is that we should not look for mere correlations between maternal condition and offspring sex but how mothers change their strategy across a range of conditions.

The second result is that mortality rates after offspring’s independence matter for the optimal sex-allocation strategy. This is in contrast to Fisher’s theory of maternal investment, which states that the period after dependence should not influence sex-allocation.

In sum, our research can explain the mismatch between predictions of Trivers-Willard theory and field data, it extends the theory to incorporate differences between females and males, and proves that mortality rates over the entire lifespan matter when deciding to produce a daughter or a son. We also show how to calculate the optimal strategy for any species…just in case you wonder what the ewe really should do.

** Also humans have been found to adjust the sex of their offspring, where “condition” is replaced by “wealth”. This can be explained by men searching (or finding?) their partners in lower salary classes, while women find their partner usually in higher salary classes. I omit a discussion of the Gender-pay-Gap (more here: http://ec.europa.eu/justice/gender-equality/gender-pay-gap/index_en.htm) and mate change frequency depending on wealth.