Tuesday, May 17th 2011

Do girls steal some of their mother’s beauty? Sex bias in parental investment

Sons and daughters and differential parental investment

One of my favorite rhetorical tricks is asking my students a question that has an obvious answer based on cultural expectations, but is wrong. So every year, when I start to teach my students about parental investment, I ask:

Who is harder to raise, sons or daughters?

I’ve asked by a show of hands and with iClickers, over the years, and the room of 750 is almost unanimous: daughters are harder to raise. So, then I get off the stage and walk around a bit. What do you mean by that? I ask.

Girls cause more gray hairs.
Girls cause more trouble when they start to like boys.
Girls are more work, and cost more money, since they shop all the time.
Girls talk back more.

And of course, there is always the saying that girls steal some of their mother’s beauty.
So then I show them this:

From Helle et al 2002.

Here is a graph of maternal longevity based on the number of sons or daughters they have. This data was based on a historical population from Finland from 1640-1870 using church records (Helle et al 2002). As you can see, the more sons mothers bear, the shorter their lifespans. You see the opposite for daughters. So sons have a negative impact, and daughters have a positive impact. This same trend has been found in records from a Flemish village (van de Putte et al 2003, 2004), where sons negatively impact lifespan but not daughters. Interestingly, data from church records from the field site where I work in rural Poland provides a slightly different picture: every offspring of either sex reduced lifespan by about 95 weeks (Jasienska et al 2006).

From Jasienska et al 2006.

Once students see these graphs, they quickly realize what is going on. Generally speaking, girls help mothers more at home in terms of chores and alloparenting. And in many cultures, particularly the historical ones studied so far, sons are costly because parents invest more in them, to help launch their own families. Daughters, not so much. In the Polish population, there may be other factors where daughter investment is important, or it is just costly to have so many offspring and you have maternal depletion regardless of daughter help.

Sex bias in parental investment is an important part of understanding both the biology and culture of parenting, and the developmental trajectories of children. The Trivers-Willard hypothesis, which has been tested many times in humans and animals, suggests that parents should invest more in sons when conditions are good, and more in daughters when conditions are bad. That is, when you have lots of resource you should put it towards a son in order to increase the chances he will have high reproductive success, since his is assumed to be more variable and high effort could lead to high reward. But in periods of low resource, daughters are a good bet because they are more likely to have at least some reproductive success no matter what.

From Hrdy 1990.

Of course, differential investment based on resources is further conflated in humans due to culture and, I would contend, our almost universal favor for patriarchy (Smuts 1995). Here is an image of an Indian family waiting at a clinic. There is a mother, an older son, and a twin boy and girl. Notice the extreme difference in health between the infant boy and girl – they are twins, yet the infant girl is emaciated. This is because in this population sons are always fed and cared for first, and whatever is left over, if there’s anything, is given to daughters.

So, parental investment can have real effects on the parent in terms of lifespan, and perhaps also their own future reproductive capabilities. Further, the conditions under which you may have children can vary, but how much a parent chooses to invest in their children varies too.

The piece of this that may be toughest to parse out, particularly in humans, is how the condition of the mother (or parents) can vary, and how that variation impacts the sex ratio of their children. In some species, like red deer, it is easier to imagine a mechanism: these animals have diapause, a period where their embryos are dormant until it is a good time to gestate and bear them. It is easier to insert some kind of selection process into a period where several embryos are all “frozen” and sex has been determined. But what about humans that produce singletons and invest huge, overlapping amounts of support to their children over decades? How would a sex bias based on maternal condition operate? And is there anything the offspring can do about it?

Changes in maternal breast size during pregnancy

It turns out that measurements as easy as stepping on a scale, and knowing your bra size, can begin to unpack the answer. First, a confession: I consider the author of this paper Andrzej Galbarczyk more than a colleague, but a friend. Andrzej is the graduate student who oversaw my Polish field site last season (Mogielica Human Ecology Study Site, director Dr. Grazyna Jasienska). He has translated consent forms and surveys for me and we’ve had many valuable and important conversations about my fieldwork. He is a smart, kind and thoughtful person and scholar. So, I let him see an early draft of this post to make sure I understood his point of view.

Galbarczyk performed an internet survey in Poland with 120 women, where he asked them to report their pre-pregnancy weight and bra size, their bra size directly after giving birth, and the sex of their offspring. He found two notable differences in these women: mothers of daughters weighed less before pregnancy, but had a greater changes in breast size during pregnancy.

The evidence about maternal pre-pregnancy weight is consistent with the Trivers-Willard hypothesis, as mothers who had sons were more likely to be heavier, and thus have more resource to invest. The second significant difference, that mothers with daughters had larger breasts after pregnancy, seems could be argued either way: Galbarczyk argues that it supports Trivers-Willard because mothers of sons could have been devoting more resource to growing their offspring rather than their breasts.

In other animals and primates particularly, mothers of male infants produce more energy-dense milk, yet mothers of female infants may produce a greater quantity of milk (Hinde 2009). And breast size is a pretty noisy signal of milk quality or quantity. So, what is the meaning of this difference in breast size?

Adaptation or physiological inevitability?

Galbarczyk suggests the difference is related to the evolutionary underpinnings of human female breasts. Women develop breasts around puberty, and though they certainly change in size and shape over time, keep them their whole lives. Other animals develop their mammary glands only shortly before lactating and then they regress again. Many contend that human breasts are an honest signal of fertility. This is at least partially confirmed by the correlation between breast size and estradiol concentrations (Jasienska et al 2006).

Galbarczyk thinks that the larger breasts seen in postpartum mothers to daughters may be a way to attract a mate for parental care. Perhaps this would help where she has given birth to the less-favored sex and needs to really convince him to participate; this could be a signal from the mother or the female fetus. Or maybe by appearing more attractive, she can have another reproductive opportunity, which would give her a chance to have a son.

You all know how I feel about evolutionary storytelling. In certain ways I do find this particular argument compelling, from the perspective of the Trivers-Willard hypothesis. But the evidence for the adaptive scenario around breast size is circumstantial.

Also, I don’t want this story to detract from some very interesting data: remember that Galbarczyk found that in this population, mothers of daughters weigh less before pregnancy, and develop larger breasts afterwards. Very cool. So perhaps we should consider a mechanistic, rather than adaptive explanation?

I have two thoughts about this, both related to androgens (androgens are the class of hormone that testosterone falls under). First, I wonder if there is an effect of fetal androgens from a male fetus on breast size. If so, mothers of daughters would have larger breasts simply because they aren’t having their breast tissue growth or density suppressed by androgens. It could simply be physiology that doesn’t have adaptive meaning.

Second, the mothers of sons were heavier before pregnancy. Heavier individuals tend to have higher circulating insulin levels, and the ovary can respond to higher insulin by producing more androgens (Poretsky 1991, Dimitrakakis et al 2004). So you could have a suppressive effect on breast size from that avenue as well. You don’t need an adaptive scenario for either of these mechanisms, just a consequence of how hormones work.

I would love to see Galbarczyk or someone else follow up on these thought-provoking results by measuring women, rather than relying on self-report, and by measuring their estradiol, progesterone and androgens. Understanding the different factors and motivations that lead to sex differential investment and outcome is a great field of study, and this work gets us thinking in a new direction.

References

Dimitrakakis C, Jones RA, Liu A, & Bondy CA (2004). Breast cancer incidence in postmenopausal women using testosterone in addition to usual hormone therapy. Menopause (New York, N.Y.), 11 (5), 531-5 PMID: 15356405

Galbarczyk A (2011). Unexpected changes in maternal breast size during pregnancy in relation to infant sex: An evolutionary interpretation. American journal of human biology : the official journal of the Human Biology Council PMID: 21544894

Helle, S. (2002). Sons Reduced Maternal Longevity in Preindustrial Humans Science, 296 (5570), 1085-1085 DOI: 10.1126/science.1070106

Hinde K (2009). Richer milk for sons but more milk for daughters: Sex-biased investment during lactation varies with maternal life history in rhesus macaques. American journal of human biology : the official journal of the Human Biology Council, 21 (4), 512-9 PMID: 19384860

Hrdy, S. (1990). Sex bias in nature and in history: A late 1980s reexamination of the “biological origins” argument American Journal of Physical Anthropology, 33 (S11), 25-37 DOI: 10.1002/ajpa.1330330504

Jasienska G, Nenko I, & Jasienski M (2006). Daughters increase longevity of fathers, but daughters and sons equally reduce longevity of mothers. American journal of human biology : the official journal of the Human Biology Council, 18 (3), 422-5 PMID: 16634019

Poretsky L, Seto-Young D, Shrestha A, Dhillon S, Mirjany M, Liu HC, Yih MC, & Rosenwaks Z (2001). Phosphatidyl-inositol-3 kinase-independent insulin action pathway(s) in the human ovary. The Journal of clinical endocrinology and metabolism, 86 (7), 3115-9 PMID: 11443175

18 Comments

  1. Anonymous said:

    Very interesting; I enjoyed reading this.

    -Rainee

  2. Matt said:

    Kate
    Excellent piece.
    I was wondering tho … for our culture with the lower number of children per mother, isn't the students' answer correct. Looking at the data, for say 2 sons and 2 daughters, the mother has a longer life expectancy for having 2 boys (74 years vs 72 years).

  3. Martha Joy said:

    My first thought about bra sizes: That's not objective. I have changed my bra size considerably when I changed shops, even though I have not lost or gained weight. I have used both 85C and 65F in the same month. But the 65F fit better.

    The image of the Indian family makes me cringe.

    Your graphs are very hard to read, and I can't make them bigger on my screen. They're blurred and useless, sorry. Something you can do about that?

  4. John McVey said:

    It may be that unmarried daughters, in some times and places, could be depended upon to care for elderly parents. Daughters-in-law, too, of course (I'm thinking of Japan). Hence, contributing to longevity of the parent(s).

  5. KBHC said:

    Thanks, all. Matt, that might be right for particular data points. The very different trend with increasing numbers of sons or daughters, though, is significant.

    Martha, I have similar concerns about the method. But Galbarczyk does show that it is a validated method, and even if there is variation based on where you get measured, likely mothers of sons and daughters would be equally off. So, that would explain why you could still find a relationship. As for the graphs: if you click on the image it does get bigger. You can also download them on to your computer to zoom in. I am sorry you find them “useless.” I have to balance the appearance of the post with the size of the images.

    John, yes exactly! I'm guessing even married daughters would help in some circumstances. In general, caretaking by women happens in lots of ways. Probably having daughters eases the burden of all caretaking by the mother.

  6. Martha Joy said:

    I'm sorry for sounding crass. I tried clicking and enlarging earlier today, and it didn't work. Now it's fine. Although I can't use the zoom-function, I have to ctrl++. I think you could probably make them larger in your post as well, though. But that's up to you.

  7. GMP said:

    What a great post! Thank you.

  8. praprotnik said:

    Very interesting post! I really liked your mechanistic explanation.

  9. KBHC said:

    Thanks GMP and praprotnik :).

  10. Anonymous said:

    Really interesting post!

    I wonder whether studies like these could be done in mammals who don't rely on assistance from daughters for childcare? That might help to distinguish between the cultural/adaptive and hormonal hypotheses.

    -Principle Investigator

  11. Anonymous said:

    If it counts for anything, everyone I've ever talked to thinks girls are _much_ easier to raise than boys . . . I've never heard of anyone saying the reverse!

  12. Girlpostdoc said:

    Great post.

    In your first graph, how many children (grandchildren) did the boys have and how many did the girls have? If daughters have more kids then increased lifespan of their mothers may be reflective of simple investment in ensuring their longterm fitness.

    As for breast size…I would again think in terms of long-term fitness.

  13. Anonymous said:

    I would be very cautious about the breast size thing. There is great variation with breast sizes before, during, and after pregnancy and also before, during, and after weight gain of any kind. I have never heard of the gender of a baby playing a role in the pregnancy portion, and it sounds way too complex to be even mainly influenced by that one factor.

  14. KBHC said:

    GPD, that's a great question but I have no idea whether they have the data to tell that! I would assume they have it, maybe in another paper that I haven't seen :).

    Most recent anon, yes, that's why it's not the best measure, but they did find a statistically significant difference between mothers of sons versus daughters. That lends at least a little credibility to the method. Variability doesn't mean you can't find a difference, and I don't think the author was asserting the sex of the fetus is the only factor.

  15. Anonymous said:

    I know I'm a little late to the game here, but I have a question. Sex of a fetus is determined by the sperm and I tend to think that this suggests that the sex of the fetus has some probability of being XX or XY (or XXX, XXY, etc although those are much rarer) depending on the proportion of X and Y sperm that the men produces (which probability should be randomly distributed across women of all weights in the study).

    So why would pre-pregnancy heaviness correspond to producing male fetuses?

    Is the idea that because of the plenty of the environment, that female fetuses would be more likely to be spontaneously aborted at a very early stage of development?

    Or would the plenty of the environment give some advantage to the Y sperm at the expense of the X sperm?

  16. rich lawler said:

    Interesting post on the sex-biased investment stuff. In some situations, due to cultural perceptions of “low class,” you find families heavily investing in daughters at the expense of sons. This is observed in Hungarian Roma and the Mukugodo of Kenya. Daughters can “marry up” and into a higher class by marrying non-Roma or non-Mukogodo respectively. Given this, parents in these groups invest in daughters and often give little attention to the males. This is sex-biased investment but it doesn't necessarily conform to a Trivers-Willard scenario, since mother's condition doesn't really matter.

    Regarding the T-W hypothesis, I like Hrdy and van Schaik's observations (1991 Am Nat) that show how the T-W hypothesis can be reversed when dominance hierarchies and female philopatry are in place (as is often the case in many female cercopithecines). High-ranking females, who are in good condition, are biased to produce daughters, since these daughters can inherit their mother's high rank and reproduce early; however, low-ranking females, who are in poorer condition, should produce sons, since these sons can disperse and “try their luck” elsewhere. I wonder if this occurs in any human societies…probably not.

  17. KBHC said:

    Hi Anon, thanks for the question. The mechanism could be hidden somewhere in the proportion of X vs Y sperm, but like you said, I'm guessing there isn't much variation in what men produce based on their partners (though, who knows? Sounds like a dissertation to me!). As for how it relates to pre-pregnancy weight, I'm not totally certain. There are a few differences in human fetuses based on sex, regarding the amount of hCG they secrete and the rate at which they grow. Males, on average, produce less hCG than females, and they are also slightly more likely to be spontaneously aborted very early on. However, once things are established, they do tend to grow more quickly and are slightly heavier at birth. The answer is hidden in there somewhere.

    Rich, I agree with you about the variation in investment and Hrdy's take on Trivers-Willard. Right now I can't come up with any human societies with the kinds of investment patterns you're describing, but I wonder if it would make sense to look at some populations that have high sex-selective abortion rates (China, India).

  18. Anonymous said:

    Boys are definitely easier and I believe cheaper to raise. I had one of each, and my daughter was more stressing, picky, complained (still does), needy, all about me-me-me and wants and needs the best of everything and everything everyone else has.

    My son was picky with his eating, would always give in to allow my daughter to have what she wanted because “she needs more stuff”, would wear what I bought as long as it fit and he fit in, name on the label or price tag was not the life or death matter of the hour.

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