People often ask me whether natural selection continues to operate on modern humans in industrialized societies, even though technology has liberated so many from hunger and early death. My answer is always an unambiguous "Yes!"
A recently published paper illustrates a dramatic episode of selection that happened in China a mere 50 years ago, the effects of which continue to reverberate through Chinese society. It's an example that further illustrates how selection in the sex ratio is always happening, even in the most privileged modern societies.
The paper reports data from a massive retrospective survey of the fertility of 300,000 women in China, including what must be a pretty good estimate of the sex ratio of babies to women between 1938 and 1982.
What staggered me, as it did Shige Song who wrote the paper, was a massive drop in the proportion of male births. Something happened in China in the early 1960s that massively changed the sex ratio.
That "something" was a famine -- probably history's largest. Between the end of 1958 and the start of 1962, the ill-conceived economic initiatives of the Great Leap Forward led to a China-wide famine that killed 20-30 million people.
The famine also caused a precipitous drop in the number of births, as women of child-bearing age starved and were unable to conceive or carry their fetuses to term.
These results imply a human tragedy so immense it defies my ability to describe. But they also illustrate an important aspect of evolutionary biology that remains relevant even in the most modernized societies.
Sex ratio and selection
The ratio of males to females in a population, including the human population, is always under selection. That's because if one sex becomes rare, that sex experiences less competition come mating time. So parents who can bias conception -- or even the care they invest in their young -- toward that rarer sex will, in time, have more grandchildren.
In most species, this effect of competition keeps the sex ratio close to even. But that doesn't mean every family should benefit equally via sons and daughters.
For one thing, in most mammals it takes more effort to raise a successful son who will go on to hold a territory and be a successful breeder. But raising such a successful son is like winning the evolutionary lottery.
That's why a red deer doe in good condition is more likely to give birth to a son -- who has a good chance of growing big and winning dominion over a harem -- than a daughter. Whereas mums-to-be who are in good enough condition to carry and care for a fawn, but not in the peak condition likely to yield a future king of the forest, tend to have daughters.
This is the Trivers-Willard effect, one of the most original and powerful ideas to emerge from modern evolutionary biology. It has been confirmed in hundreds of studies from wasps (where more care makes better females) to horses.
In mammals, it seems conditions in the womb might affect the survival of male or female embryos. Certainly when in-vitro fertilized cattle embryos are reared in a glucose-rich medium, only males survive, but female embryos thrive on less rich media.
Trivers and Willard actually came up with their theory by thinking about humans. Trivers mentioned to a class he was teaching that girls often marry upward into families of higher status and greater wealth. When this happens, there are too many girls competing for the wealthiest boys. And too many poor boys competing for the few poor girls who haven't already married up.
Willard -- a student in the class -- suggested wealthy families might benefit from biasing conception or investment toward sons, and that poorer families should do the opposite. Crucially, the effects of too many boys born into wealthy families and excess girls in poorer families would balance out, leaving the overall sex ratio approximately equal.
Evidence suggests this is exactly what happens. Some 60% of the children born to billionaire families are sons. If that ratio was repeated Australia-wide, men and boys would outnumber women and girls by about four million.
Junior wives in polygynous Rwandan marriages suffer low status and often agonising poverty, and they have overwhelmingly more daughters than higher-status first wives or the wives of monogamously married men.
Trivers-Willard effects manifest after children are born too. In the pre-industrial German parish of Leezen, sons in wealthy land-owning families were far more likely than their sisters to survive to their first birthday, whereas the opposite was true in poorer families. That's probably due to subtle, even subconscious, differences in how parents fed and cared for their sons and daughters.
The Great Leap Forward
If the mechanisms underlying Trivers-Willard effects are aligned -- as we suspect -- with nutritional conditions, then we might expect dramatic sex ratio fluctuations when a whole population experiences extreme food shortage.
Yet studies of two of the 20th century's most dramatic famines -- the Dutch Hunger Winter of 1944-5 and the 1942 Leningrad Siege -- showed equivocal associations between famine and sex ratios. Crucially, these famines lasted seven and six months respectively -- enough to kill vast numbers of people but perhaps not long enough to bias the birth of an entire cohort.
It's also possible that the least-starved mothers, deprived as they were, produced sons because they were in relatively better condition than the other mothers.
Trivers-Willard effects often seem to be relative. Only the very wealthiest and highest status families experience the strong bias toward having more sons, irrespective of their absolute level of wealth. That would explain how billionaires could have dramatically more sons than mere multi-millionaires. And that might explain why the sex ratio doesn't bounce around too dramatically from year to year, responding to lean and fat years.
But Song's paper, published last week, shows that a long-lasting, severe famine can change the sex ratio at birth. Both birth rate and sex ratio headed south about a year into the famine and remained there until about two years after the famine ended.
It seems that for the Trivers-Willard effect to bias the sex ratio of an entire cohort, the famine must last for some time before the onset of pregnancy.
And presumably the drop in birth rate comes from male embryos and fetuses faring worse than females during famine, either failing to implant, or miscarrying at higher rates.
China's sex ratios are notoriously male-biased and becoming more so, but the worst famine in history created one tiny cohort in which almost as many girls were born as boys.