In a 2012 article that was published on the ISET Economist Blog, Yaroslava Babych did justice to what lately has been a theme of scientific gossip and backstage talk, which I have personally often encountered among socially (albeit not exclusively) inclined economists about the alarming sex ratio at birth (SRB) statistics in Georgia and its neighboring countries. Yaroslava Babych presented numbers showing that SRB—the ratio of boys to girls in a baby population— of Georgia is topped just by China, Azerbaijan, and Armenia.
Judging from the number of comments that followed, the blog proved popular as it generated a lot of attention and sparked a healthy discussion about potential causes of the problem. People engaged in the discussion suggested all sorts of explanations, varying from preferences of males over females and sex selective abortions to the “returning soldier effect”, parental stress as well as the country specific diet. This article however, intends to give an alternative perspective on the topic, which I think will enrich the discussion.
In the early 1990s Jaroslav Felgr, an evolutionary biologist at Charles University in Prague and a collaborator of mine, started to analyze the influence of a particular single-celled brain parasite on human behavior. This parasite of protozoan family known as Toxoplasma gondii (or Toxo) was discovered in 1908 in the body of the exotic rodent Ctenodactylus gundi (hence the name gondii). Flegr advocates that Toxo is the classic exhibition of the manipulation hypothesis, which maintains that parasites have an ability to alter behavior of their hosts in order to maximize the chances of transmitting of their own genes across generations. The definitive hosts of Toxoplasma are animals from the cat family or felines — the only species in which parasite reproduce sexually. In contrast, any warm-blooded animal (mostly rodents such as rats, mice) can become infected as a fetus or after birth by feeding on food contaminated with feline excrement infected by the parasite. In order to close the evolutionary cycle, Toxo faces the challenge of getting a rodent to be eaten by a cat. To do so, Toxo devised a powerful strategy: it began to manipulate its host’s brain so that the smell of predator urine sexually aroused rodents, therefore removing their instinctive fear of cats and making them lethargic. Sluggish rodents then go around exploring the cat’s urine, thereby making them easy prey — a condition called "Feline Fatal Attraction."
But what does this have to do with the sex ratio in humans? In his 2011 book Watch out for Toxo! (available for free online), Flegr claims that one-third of the world’s population has toxoplasmosis — a disease caused by Toxoplasma. Prevalence of toxoplasmosis varies dramatically across countries. It can be as low as 4% in South Korea and as high as 78% in Nigeria. In Europe, Toxo prevalence varies between 11% in Norway and 63% in Germany.
Could it be that Toxoplasma is also trying to alter humans’ senses in a way similar to rodents, thus making them behaving in bizarre ways? Flegr and his crew generated a set of results that answer affirmatively to part of this question. Toxoplasma-infected patients show slowed reaction times and face an increased risk of depression, schizophrenia, car accidents, and suicide (Flegr, J. (2013): “How and why Toxoplasma makes us crazy”, Trends in Parasitology, 29(4), 156-163). In a 2011 paper (“Fatal Attraction Phenomenon in Humans – Cat Odour Attractiveness Increased for Toxoplasma-Infected Men While Decreased for Infected Women”, PLoS Neglected Tropical Diseases, 5(11)), Flegr claims that, like rodents, infected men find the odour of cat urine increasingly pleasant. Interestingly, infected women displayed lower levels of intrigue with the smell of cat urine than uninfected women did.
Interesting as all this may be, we still haven’t answered our original question: how can Toxoplasma be influencing the sex ratio at birth? In a 2006 article, Flegr links Toxo infection to the propensity to have male or female offspring (“Women infected with parasite Toxoplasma have more sons”, Naturwissenschaften 94, 122–127). An analysis of clinical records in Prague showed that women, infected with Toxoplasma right before pregnancy had a 72% chance of giving birth to a boy, which means that there were 260 boys for every 100 girls in the population (as a quick comparison, Yaroslava Babych reported that in the South Caucasus the highest value of the sex ratio at birth is 116). According to Flegr and co-authors, there is a good evolutionary story behind observed result. In primitive societies, where men’s primary occupation was hunting, which required men to be aggressive, exploratory and willing to pursue prey over large distances, it was more likely that they would be eaten by wild felines. Therefore, the male-biased sex ratio can be seen as the parasite’s way of ensuring the completion of its evolutionary life cycle. The same study showed that for women with Toxoplasmosis that lasted relatively longer, the probability of giving birth to a son dropped to 45%. However, the evolutionary role of Toxo’s effect on the sex ratio is still debated, and the details of a biological mechanism are outside the scope of this article.
This result did not proof that Toxo was the cause of the skewed sex ratio, because it might well be that high the sex ratio at birth, as well as the tendency to be Toxo-infected, is caused by a common unobserved factor such as increased levels of testosterone. To rule out this possibility, in a 2007 study (“Influence of latent toxoplasmosis on the secondary sex ratio in mice”, Parasitology, 134(12), 1709-1717), Flegr’s team experimentally demonstrated that artificially infected mice had an increased probability (59%) of giving birth to male pups in the earlier weeks of infection. However, as time passed the sex ratio at birth has reversed and the chance of giving birth to males dropped to 40%.
After reading all of this, an astute reader may wonder, “how does this explain that in the South Caucasian countries SRB stands higher than in other countries?” Do these countries drastically differ from other countries in terms of Toxo prevalence? Do we actually know the rate of infected population in these countries? Unfortunately, I am unable to answer these last questions due to data unavailability. But even the existence of the data may not have been very informative, as previous attempts trying to link Toxo prevalence and the sex ratio at birth across countries have failed. The reason is that the main factor when linking Toxoplasmosis and sex ratio at birth is the length of infection of the mother and humans usually do not know when they contracted toxoplasmosis. But I can nevertheless speculate why I think Toxoplasmosis can be a reason for the high sex ratio at birth in the region.
It might be the case that in the South Caucasus toxoplasmosis works towards an increased rate of male babies because women get married relatively early. Indeed, the average age of mothers when giving birth in Germany is 31, while depending on the source, the average age of women at childbirth in Georgia is between 22 and 24 years. If the probability of being infected for the first time is the same throughout a whole lifespan (which is probably not true, but is a reasonable working hypothesis), then if you randomly pick a woman at age 31 and a woman at age 22, it is more likely that the women at age 31 has been infected for a longer period of time than the woman at age 22. Therefore, on average the length of Toxo infection of a mother giving birth in Georgia will be lower, making it more likely for Georgian women to give birth to sons. (In Germany the average age of birth giving women went up from 24 years to 31 years between 1965 and 2012. Therefore, if our reasoning is true and the rate of infection remained the same throughout this time, Germany must have experienced declining sex ratio at birth — a hypothesis that could be tested empirically).
Moreover, one of the causes of infection is interaction with raw meat and vegetables. It might be that, in some countries women, after they get married, spend more time cooking in the kitchen as compared to fellow housewives in other countries. Therefore, in these countries women could get infected right at the start of their pregnancy and thus give birth to more sons. Finally, toxoplasmosis can be transmitted during unprotected sex with infected men. It could also be the case that relatively large numbers of Caucasian men are infected with Toxo, which would make the share of women getting toxoplasmosis right before pregnancy relatively higher as well, thus increasing the likelihood of having male babies.
At the moment, what has been discussed above is mainly speculation. Yet in a scientific discussion about the skewed Georgian sex rate at birth, the Toxo story should be further investigated as one possible explanation.
Lasha Lanchava is a former ISET student. Currently, he is junior researcher and PhD candidate at CERGE-EI, Charles University in Prague, Czech Republic.
Comments
Interesting explanation...doesn't account however for why the sex ratio jumped only in the 1990s.
Interesting, but the shift has started in 90s, three factors technology development tendency to small family size and son preference are present in Georgia hight rates of abortions also lead us to think that unfortunately, difference in sex ratio is caused by the selective abortions
Logically then Nigeria, with a toxoplasmosis rate of 78%, should exhibit much higher ratios of boys to girls than almost any other country...but that is not the case. On the other hand, South Korea, with the lowest toxo rate, was actually one of the countries where sex-ratios were high a couple of decades ago -- driven by sex-selective abortions -- and where a public policy response slowly but surely turned things around and eventually reversed the trend. The explanation, as Tiko points out, is likely to be the most obvious one -- sex-selective abortions. The question, therefore, is why there is such an aversion to accepting that explanation rather than the infinitely more exotic ones I've heard over the past few years. Certainly, everything I've read and heard confirms that abortions are not uncommon in the South Caucasus.
MLM, I share your concern as well as thoughts of Y, that Toxo story may not have overwhelming explanatory power. Therefore, at the end of the blog, I acknowledge that proposed story is a speculation only (earlier drafts included much more extended disclaimer). This is not definitely an "excuse" article as it does not directly imply that toxoplasmosis contributes to the skewed sex ratio. It might well be the case that women in the South Caucasus get infected in early childhood, thus having the highest length of Toxo infection in the world (thus giving birth to more females). If true, then the “Missing Girls” problem would be much more severe than we currently think it is. My intention was to raise an awareness of the Toxo phenomenon which is proven to be influencing sex ratio. Therefore, I believe that, whether it will be a general discussion or scientific investigation, Toxo story need to be taken into account. You are talking about widespread usage of abortions in South Caucasus. That might be true but sex selective abortion is entirely a different concept. And unless rigorous scientific study shows the validity of either hypothesis, then any explanation would be as exotic as the Toxo story may seem.
One more observation to clinch the author's point. In Georgia it seems usual that the first baby is boy and the next could be girl.
Nigeria, which has a very high rate of Toxo infection, according to the article, has also relatively "normal" SRB - about 106 boys per 100 girls ( CIA factbook ). In the meantime, the age of mother at first birth is about 20 years old. If we believe the Toxo story and how the duration of infection affects SRB, this doesn't add up. Nigeria by this logic should have a very high SRB.
One may argue that the average number of children born to one woman in Nigeria is about 6, which means that there is a possibility of having boys earlier in life and girls later. However, for this to work it must be that SRB not only reverts to normal, but actually flips on the later stages of infection. Doesn't seem that there is evidence of that for humans. Plus, we do not know much about the threshold duration for the infection to start producing the opposite result.
Be as it may, my personal opinion is that until we do have some data on the rates of Toxo infection in the South Caucasus, maybe we should at least try to check less exotic hypotheses. Unfortunately it is not easy. Surveys are not very helpful in this respect. If the problem indeed is sex selective abortions, there is a very high chance of misreporting the true reasons for abortion.
But one thing can be checked and discussed - gender preferences in the society. In countries like India, for example, women face high social and family pressure to have boys. But what is the situation like in the South Caucasus nowadays, Georgia in particular?
I've already mentioned in the article, that Toxo seroprevalnce per-se can not be linked to SRB. What matters most is the length of toxoplasmosis. And even if women in Nigeria give birth around age of 20, one can think of plenty of reasons why these women got infected at early childhood thus giving birth to more females (or to not so much sons). You mentioned that women in Nigeria have 6 children on average. One study http://www.psychologytoday.com/files/attachments/3343/sex-ratio-birth-polygyny-and-fertility.pdf shows that there is a significant negative correlation (-0.6) between SRB and total fertility. That, together with sex ratio reversal story at later stages of toxoplasmisis (when likelihood of having boys drops to 0.45), could also explain why SRB is not very high in Nigeria.
I recently became aware of the fact that every major birth clinic in Tbilisi tests women for toxoplasmosis. The availability of the data is a problem (due to confidentiality) but interested parties may get a hand on it and easily put an end to the speculation.
About your last point I would say that in Georgia there may not be as high pressure on women to have boys as in India and China. And even if a survey shows very high son preference in Caucasian countries, it will not necessarily imply that parents practice sex selective abortions. I know many couples who had a girl as a first child but they wanted a boy and they keep having children until they reach a goal. Sometimes they give birth to 3-4 females.
Lasha, just to make sure I get it right: your argument seems to imply that women in Nigeria get infected with Toxo in early childhood, but women in Georgia get infected closer to their childbearing age. Why is that?
Another question (I couldn't download the article your referenced, I am assuming this information is there) - how much longer does the woman have to be infected for the likelihood of having a boy to drop to 45%?
Here's another hypothesis! From the study "Human sex ratio at birth in South West Nigeria" http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3168160/
"Data also indicates more male birth in the rainy season, suggesting a seasonal variation of sex ratio."
It's raining men
I already argued/speculated in the blog why I think women get infected at the start of pregnancy in the South Caucasus. Why would women in Nigeria get infected in early childhood? Some statistics (from CIA factbook) can help here: Drinking water source: 61.1% in Nigeria, 98.1% in Georgia. Sanitation facility access: 30.6% in Nigeria, 93.4% in Georgia. Degree of risk of major infectious diseases: very high for Nigeria, not cited for Georgia. Given these, it is easy to imagine why Nigerian children would be more vulnerable to Toxo infection.
The article I was referring to seems to be working for me. You may try to search it via title: Sex Ratio at Birth, Polygyny, and Fertility: A Cross-National Study. As I know we can not exactly assess how long a person has been infected with toxoplasmosis. We can just proxy the length of infection by the level of concentration of Toxoplasma antibodies in serum.
The article you referred to eventually does not find a significant effect of seasonal variation on SRB. In general, I would be reluctant to use these kind of studies as a reference given the impact factor of a publishing journal http://www.researchgate.net/journal/0971-6866_Indian_Journal_of_Human_Genetics .
Ok, I found the article I was looking for (“Women infected with parasite Toxoplasma have more sons”, Naturwissenschaften 94, 122–127) . One note - this article cannot be used as evidence to support the SRB reversion story.
Page 125 panel (a): the real value for SRB at very low titre values (longer infected women) is indeed 0.45, but the errors are very large. As authors themselves point out:
"In high-prevalence countries, most women of reproductive age have already been infected for a long time and therefore have only low titres of anti-Toxoplasma antibodies. Our results suggest that low-titres women have similar sex ratios to Toxoplasma-negative women." (page 126 paragraph 5)
I did not say that reversion story is the only explanation. I said it would work in tandem with the evidence that there is a negative correlation SRB and total fertility.
The main explanation I offered, for not very high SRB in Nigeria, was that childbearing women have relatively longer periods of infection. And if you believe your last quote, then it becomes clear why, in countries like Nigeria, we may not observe unusually high SRB.
Interesting...so the idea is that Nigerian women get infected so early, that by the time they give birth their SRB is normal, while in Georgia women would get infected in the early years of marriage and their firstborns would be overwhelmingly sons...
Ideally to see if this may be true for Georgia case, one would need to check SRB by birth order of the child. While there is such statistics for Armenia, I cannot find it for Georgia. The only statistics I can find is Live Birth by Sex and Age of Mother from Geostat http://www.geostat.ge/index.php?action=page&p_id=1091&lang=eng
After checking several years, it seems that if anything SRB increases slightly with the age of mother...
If we exclude teenage moms then the graph shows that number of boys and girls converge as the age of mother increases, right?
The graph you see is a bit misleading. It is for one year only and scale sensitive, as it graphs the numbers of male and female births, not the ratio between them. If you download the excel file and calculate SRB for all years you will see the pattern I am talking about.
The Nigeria vs Georgia explanation works for me. But what about the earlier period in South Caucasus history? What changed? One answer is that the birth rates dropped as a whole because this was the wrong time to have the second or third child. This would suggest that the average mothers' age declined after 1991. Would that help? It might, because older women are more likely to have older Toxo infection and normal or even reversed SRB.
I may be wrong, but think the statistics should be "mean (average) age of mother at birth of first child", not "average mother's age" (I have not seen the latter formulation anywhere).
It is very true that birth rates declined dramatically in the 1990s. So if we believe that firstborns are much more likely to be sons than daughters, whatever the woman's age, then your explanation would hold.
However, from what I have seen in the literature it seems that SRB in the 1990s decade was the highest for the third-born - and for the third-borns SRB has been indeed increasing quite sharply since the 1990s.
Is that literature referring to Georgia? According to Geostat, the share of third born children is about 8% for 2003 in Georgia (that's the earliest date for which birth order data is available). Therefore, even if there were very high number of third born males than females, that can not account for the dramatic shift in overall SRB.
That's a very good hypothesis Eric. Indeed, according to Geostat data the number of births dropped from 92000 in 1990 to 72000 in 1992 (more than 20% decrease) and to 61000 in 1993. In subsequent years number of births further kept decreasing until it reached the lowest value of 46000 in 2003.
Actually, the fact that there was a dramatic shift in SRB in early 90s makes me suspicious to abortion story. I can not think of good answer to why would people suddenly decide to practice abortion more frequently.
http://paa2004.princeton.edu/papers/40166
Here's the paper I was referring to. (page 3). If ratio at third birth is very high, and elevated at second, it could still result in an elevated overall ratio. It should be easy to check.