Why is the human sex ratio 1:1 at birth?

Having found a dramatic shift in sex ratio at birth in one species of mammal, I have for decades kept an eye on discussions as to whether the human sex ratio at birth differs in some circumstances from 1 male: 1 female. Mammals in theory have two ways of controlling the sex ratio at birth: (i) at conception, or (ii) later by selectively reducing the number of young in utero. We found the latter mechanism at work in the guinea-pig. Since human litter size usually equals the  number of eggs and rarely exceeds 1 and since gestation is relatively long, it always appeared that if there were to be any maternal or paternal genetic control of the sex of the offspring it would have to be at the time of conception, rather than by selective death and reabsorption of embryo or fetus.

In the 1980s I once did the experiment of asking biologists from different disciplines why they thought the human sex ratio is 1:1. The reproductive biologists replied that it was just the result of random segregation of the sex chromosomes. The sex of a human offspring depends on whether it inherits and X or a Y chromosome from its father. Random segregation will, on average, result in a 1:1 ratio. By contrast, the evolutionary biologists said that the sex ratio is explained by Sir Ronald Fisher’s Principle: with the sex of a subject to genetic variation, the the sex ratio will always stabilise at 1:1. I will not repeat the simple explanation that can be found here.

Shifts of the of sex ratio at birth in various animals has been explained in terms of the Trivers-Willard hypothesis: parents which possess a heritable trait that benefits the lifetime reproductive success of one sex will bias the sex ratio towards that sex. There have been various claims in studies of human populations along these lines; for example, male-biased sex ratios in taller, wealthier, high status parents with the offspring likely to be more successful in competition for a mate. However, such claims have been controversial because of the statistical methods used and the results have often not borne out when larger samples were taken from the population.

Both the Fisher Principle and Trivers-Willard rely on there being genetic variation in the sex ratio, in other words that a bias towards one sex or the other is heritable. Thus a key test is to look for heritability in a very large human population. On standard scale of 0 to 1, ‘0’ denotes that a trait is not heritable while ‘1’ all differences in a trait can be explained entirely by genetic variation. Many traits fall somewhere between those two extremes.

But what does determine human sex ratio? It would be predicted if sex ratio is a heritable trait then Fisher’s Principle would apply. By contrast, if it is not heritable then simple Mendelian segregation of the sex chromosomes would suffice as an explanation.

Over the years there have been all sorts of suggestions and claims that the tendency in a family to produce offspring completely or partially biased to one sex is hereditary, and that particular genes could be involved. However, these conclusions have been criticised because the sample sizes were small and the statistical inferences drawn were invalid.

A recent, important paper has tackled the problem by using data from the entire population born in Sweden in and after 1932. That was 3,543,243 individuals and their 4,753,269 children. The results of the analysis were clear. There was no evidence of heritability at all. The calculated heritability was 0. In other words, there was no need to invoke Fisher’s Principle since with no heritability there can be no Fisher.

The authors summed up their results:

In sum, all of our results are consistent with the simple explanation that variation in offspring sex ratio in humans is due to unbiased Mendelian segregation of sex chromosomes during spermatogenesis and unbiased fertilization. The slight excess of male births is likely to be due to a general difference in survival of male and female embryos in the womb, the reasons for which are not yet understood.

Looks like my reproductive biology colleagues were right. Pity I can’t tell most of them; they are long dead.

The question now, of course, is whether the same conclusion, that the human sex ratio at conception is simply the outcome of random segregation of the sex chromosomes, applies to other or to all mammals? And are the statistically-robust demonstrated shifts in sex ratios at birth in some species and in certain environmental conditions all the result of differential loss of embryos and fetuses in utero? I shall permit myself to guess that the answers are ‘Yes’ and ‘Yes’ even though, as with previous human studies, there have been claims that the answer to the first question is ‘No’.

Zietsch BP, Walum H, Lichtenstein P, Verweij KJH, Kuja-Halkola R. 2020 No genetic contribution to variation in human offspring sex ratio: a total population study of 4.7 million births. Proceedings of the Royal Society B 287: 20192849. http://dx.doi.org/10.1098/rspb.2019.2849

Peaker M, Taylor E. 1996. Sex ratio and litter size in the guinea-pig. Journal of Reproduction and Fertility 108, 63-67.

‘I believe it to be impossible to breed genuine wild animal under artificial conditions as to stand in a bucket of water and pick oneself up’. Helen Spurway’s original and neglected work from 1952

The breeding of wild animals in captivity is managed to maintain genetic diversity. Everybody knows that from television programmes on zoos, even after stripping out the anthropomorphic claptrap of the populist commentary. But even with the best management there is a limit to the number of generations that small populations can be maintained without incurring the deleterious effects of inbreeding. And when it comes to reintroducing populations into the wild is the gene pool the same as that in the original wild population? In other words, has there been artificial selection, however unintentional, so is the captive population genuinely wild?

There have been many papers and books written on this aspect of conservation biology but none that I have seen give credit to the person who drew attention to the problem nearly 70 years ago.

Under the provocative title, Can wild animals be kept in captivity?, Helen Spurway questioned not whether wild animals can be kept in captivity from the technological point of view but whether they can be maintained wild genetically. The emphasis was thus on the word ‘wild’. She wrote:

I believe it to be impossible to breed genuine wild animal under artificial conditions as to stand in a bucket of water and pick oneself up.

She argued it was inevitable that artificial selection occurs at all stages of keeping wild animals in captivity and that everybody doing so was involved in a process of domestication:

We, who keep animals, either as amateur naturalists, curators of zoological gardens, or academic biologists, cannot help taking part in some domestications.

In her admittedly rambling article (sadly, a model of organisation compared with ones she wrote on her studies of newts), Helen Spurway, considered the genetic and environmental factors that take place in captive populations which in the end produce animals different from those in the wild.

In a nutshell, artificial selection can—and did—occur at just about every stage. Captured individuals may have been may weakest or slowest in a population. The first, or only, individuals to breed in captivity would have led to selection of those least affected by stress to pass on their genes. I could continue in the same vein but the message is clear.

Helen Spurway also pointed out that even the first breeding in captivity involve inbreeding (think Golden Hamster, with only one mother and litter forming the captive/domesticated population for decades) or a degree of outbreeding never encountered in the wild. Therefore, she argued, there is an inevitable domestication of wild animals in captivity with succeeding generations and we end up with a phenotype adapted to life in captivity rather than life in the wild.

Helen Spurway (1915-1978) was a geneticist, then working at University College London. She is best remembered as the second wife of J.B.S. Haldane who shared his marxist beliefs and admiration for Joseph Stalin. They left Britain to work in India in 1956. At the time she wrote the article she was working on genetic differences between populations of European newts and was keeping a number in captivity for breeding experiments. I have written a little about that work here.

Helen Spurway and JBS Haldane in Calcutta

But how did I get to know about Spurway’s article? In 1959, starting ‘A’ level zoology and botany, we were introduced to the Biology Library at school (where a number of us hung out for much of the day in the company of museum specimens and a human skull. The senior biology master James J Key looked towards a small pile of paperbacks and suggested we work our way through them. They were old issues of Penguin New Biology and the first one I picked up contained the article by Helen Spurway.

Penguin’s series, New Biology, was published from 1945 until 1960 in 31 volumes. It was aimed at VIth form pupils and first-year undergraduates. The ‘new’ before ‘biology’ indicated several trends, not simply the promotion of then new areas of discovery, like cell biology, over traditional descriptive pursuits such as comparative anatomy. The great, and supposedly new, emphasis was on the use of biology in human affairs. The ‘new’ in this instance represented the views of the large number of marxist and communist biologists in the British university system who were arguing that progress could only come be made by having a planned economy with planned and centrally-controlled science as part of that process. I cannot help but point out that the holders of such beliefs were horrified if anybody tried to tell them what research they should be doing. Some scientists are more equal than others.

The editors who founded and ran Penguin’s New Biology were the husband and wife team, Michael Abercrombie FRS (1912-1979), the famous cell biologist and experimental embryologist, and Minnie Louie Johnson (1909-1984). 

The history of Penguin’s New Biology is told by Sir Peter Medawar in his biographical memoir on Abercrombie for the Royal Society, which, incidentally, contains acidic observations on some of the academic zoologists of the day:

It was an important event for the Abercrombies when Lancelot Hogben succeeded Munro Fox as the Mason Professor of Zoology at Birmingham and appointed Michael [Abercrombie] Lecturer in Zoology. Hogben lived with the socio­logist Professor Sargant Florence in the top floor of whose house the Aber­crombies had a flat. Hogben and the Abercrombies became very thick and it was Hogben, a great popular educationalist (cp. Mathematics for the Million) who turned the Abercrombies’ thoughts to one of the most important enter­prises of their lives… 

Hogben arranged an introduction to Allen Lane of Penguin Books and the Abercrombies undertook to produce a series of volumes to be called New Biology, each one of which would contain a number of authoritative essays at a pretty high academic level—sixth form and university first year. Lane paid £75 for the first volume, a sum which the Abercrombies shared out among the contributors, characteristically leaving themselves out. The first volume was a great success and sold something like 100,000 copies—a great success by scholarly standards—but as the series continued to a total of 31 volumes the sales dwindled to 20 000. Eventually, then, the verdict of the market place brought the series to an end… 

New Biology had a profoundly stimulating effect upon sixth formers and first year undergraduates and probably played an important part in speeding up the recruitment into biology that caused it to take up its present position as the most deeply absorbing and rapidly moving of all the sciences today.

New Scientist on 31 March 1960 in covering the demise of New Biology concluded:

New Biology has died because it could not make a living. There is something disturbingly wrong with a culture that could allow this to happen.

There was also this cartoon:

Nowadays, Penguin’s New Biology has been largely forgotten, copies in university and school libraries thrown out along with other key volumes in the battle for shelf space. As well as crackingly good articles its pages contained some notable spats between famous savants of the day and started some controversies that ran through biology and its history for decades.

Medawar PB. 1980. Michael Abercrombie 14 August 1912—28 May 1979. Biographical Memoirs of Fellows of the Royal Society 26, 1-15

Spurway H. 1952. Can wild animals be kept in captivity? New Biology 13 (edited by M Abercrobie and ML Johnson), 11-30. London: Penguin

Spurway H. 1953. Genetics of specific and subspecific differences in European newts. Symposia of the Society for Experimental Biology 7, 200-237

Red-heads and Black-heads. New research finds the gene controlling head colour in the Gouldian Finch

The Gouldian Finch (Chloebia or Erythrura gouldiae) is famous for a number of reasons. The first is a sad one. It has become rare in its habitat of tropical northern Australia because of agricultural practice (burning grassland at the wrong time of year and the introduction of domestic livestock in areas which reason indicates should actually be left wild). The second is that it occurs in three colour morphs in the wild. The third is that because of its beauty it has always been a popular bird with aviculturists in Europe, North America and Japan.

The third reason (i.e. its popularity in aviculture) is responsible for the generation of so much knowledge about this species which has been put to good use in devising conservation measures  in the wild by halting, apparently, the precipitous decline in the size of the population and, even though only a few thousand birds of this small seed-eating bird remain, the possibly unwise lifting of its status from ‘Endangered’ to ‘Nearly Threatened’.

The breeding and maintenance of stocks of the Gouldian Finch in aviaries has also facilitated the recent discovery of the genetic mechanism responsible for the difference in head coloration of the morphs. For this article I am going to ignore the orange-headed morph which occurs at very low frequency (less than one in a thousand individuals). In the wild, the ratio of black-headed to red-headed individuals is 7:3.

From Toomey et al. 2018

Thanks to breeding records in captivity, it has been known for many years that the genetics of head colour can be explained by simple sex-linked Mendelian inheritance with the allele for red being dominant and black recessive. In 2016 this Red gene was located on the Z chromosome. In birds, the sex determination is not the same as in mammals. Male birds have two Z chromosomes, females one Z and one W.

Before going on to describe the very recent genomic work, I should point out that there are differences, discovered, again, by research on birds in captivity between the two colour morphs, in addition to the differences in head colour. Red heads are more aggressive and dominate in encounters with black heads. In competitive social environments, red heads show increased concentrations of testosterone and corticosterone in their blood whereas black heads do not. There is also assortative mating, red heads prefer red heads, blacks black. Clearly, whatever the genetic mechanism it is pleiotropic, i.e. affects a number of traits within the body.

A group of authors from U.S.A. and Portugal have now tracked down the locus of Red gene to a small region on the Z chromosome. The gene itself is on part of the chromosome that does not encode a protein that can be responsible for its actions in the body. However, it is in a position to control a nearby gene that encodes for the protein, Follistatin, and indeed the group provides evidence that it is the production of Follistatin which controls head colour as well as the other physiological traits. There is also evidence that Follistatin could be involved in controlling the differences in plumage colour between other species of bird.

There is still much work to be done on the ‘how’ or mechanistic questions as well as the ‘why’ questions such as why, given the stroppiness and dominance of the red-head over the black, the overall ratio of 3:7 has remained unchanged.

Finally, since you ask, have I ever seen in Gouldian Finch in the wild? No. Even though I have been to northern Australia several times and passed through their known range, I have not had the chance to go to one of the known hot-spots of the remaining population.

Toomey MB, Marques CI, Andrade P, Araújo PM, Sabatino S, Gazda MA, Afonso S, Lopes RJ, Corbo JC, Carneiro M. 2018 A non-coding region near Follistatin controls head colour polymorphism in the Gouldian finch. Proceedings of the Royal Society B 285, 20181788. http://dx.doi.org/10.1098/rspb.2018.1788

Legge S, Garnett S, Maute K, Heathcote J, Murphy S, Woinarski JCZ, Astheimer L. 2015. A landscape-scale, applied fire management experiment promotes recovery of a population of the threatened Gouldian Finch, Erythrura gouldiae, in Australia’s Tropical Savannas. PLoS ONE 10(10): e0137997. doi:10.1371/journal.pone.0137997

Classic Reads:

Mike Fidler (who has made enormous financial and practical contributions to the conservation and study of the Gouldian Finch in Australia an UK) and Stewart Evans (1936-2010) late of the University of Newcastle, UK. The Gouldian Finch. 1986. Blandford Press.

Derek Goodwin (1920-2008). 1982. Estrildid Finches of the World. London: British Museum (Natural History) and Oxford University Press.

Gouldian Finches have been kept and bred since the 1870s. This drawing
illustrates an article on cage-bird traffic of the U.S.A. by Henry Oldys
published in the Yearbook of the U.S. Department of Agriculture 1906