When does heritable low fitness need to be explained?

Epistemic status: speculating about things I'm not familiar with; hoping to be educated in the comments. This post is a question, not an answer.

ETA: this comment thread seems to be leading towards the best answer so far.

There's a question I've seen many times, most recently in Scott Alexander's recent links thread. This latest variant goes like this:

Old question “why does evolution allow homosexuality to exist when it decreases reproduction?” seems to have been solved, at least in fruit flies: the female relatives of gayer fruit flies have more children. Same thing appears to be true in humans. Unclear if lesbianism has a similar aetiology.

Obligate male homosexuality greatly harms reproductive fitness. And so, the argument goes, there must be some other selection pressure, one great enough to overcome the drastic effect of not having any children. The comments on that post list several other proposed answers, all of them suggesting a tradeoff vs. a benefit elsewhere: for instance, that it pays to have some proportion of gay men who invest their resources in their nieces and nephews instead of their own children.

But how do we know if this is a valid question - if the situation really needs to be explained at all?

For obvious political and social reasons, it's hard to be sure how many people are homosexual. Note that we are interested only in obligate homosexuality - bisexuals presumably don't have strongly reduced fitness. The Wikipedia article doesn't really distinguish obligate homosexuality from bi-, pan- and even trans-sexuals. The discussion in the SSC comments used an (unsourced?) range of 1%-3%, which seems at least consistent with other sources, so let's run with that.

The rate of major birth defects in the US, as reported by the CDC, is also about 3%. This counts both developmental and genetic problems, and includes everything from anencephaly (invariably fatal) through Down syndrome (severe but survivable) to cleft palates (minor). But most of these, at least 1.5% of births, were always fatal before modern medicine, and many of the others reduced fitness (via mate selection, if nothing else). Various other defects and diseases, which only manifest later in life, are also thought to be influenced or determined during early development. And so is sexual preference.

(Whether homosexuality is a developmental disorder is not the point; I'm comparing the effect of selection pressure on fatal teratology with its effect on reduced-fitness homosexuality.)

Embryological development is a complex and fragile process, and there are many ways for it to go wrong. We don't wonder how it is possible that selection pressure allows anencephaly to occur in 1 in 4859 births. There are certainly direct causes of anencephaly, explanations of why it happens when it does, but (I think) we don't a priori expect them to be due to tradeoffs yielding benefits elsewhere. It's just as plausible that the tradeoffs involved are against even worse (counterfactual) problems elsewhere - or that there are just no available mutations that don't have these or equally severe problems.

Could it be that linking sexual preference to the biological gender is, for some complex developmental reason, fragile enough that it goes wrong despite all selection pressure to the contrary, that it has no redeeming qualities from the viewpoint of evolution, and that is all there is to it?

When faced with any phenotype with reduced fitness, how can we judge if there is something to be explained - a beneficial tradeoff elsewhere to search for - or merely a hard problem evolution couldn't solve completely? And is there a way to quantify this question, relating it to the known mathematical models of genetics?


Notes:

1. I'm posting this in the spirit of recent suggestions to post more and accept lower quality of (our own) posts to Discussion.

2. I'm going to sleep now and will start replying to comments about 10 hours from now; sorry for the inconvenience.

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As far as I can tell from a brief look at the paper, it makes no attempt to estimate whether the increased fecundity of the female relative is enough to compensate for the reduced fecundity of the homosexuals. In fact, I didn't see it give any estimate for the latter. They merely do a p-test and pronounce the differences "significant". This is a situation where we are primarily interested in the magnitude of the effect, not merely finding evidence that it is positive.

Right--as well, the standard complaint about extending this logic to humans is that the most credible increased fertility effect for female relatives is desire-based. But it's easy for women to get pregnant more frequently and have more children--the hard part is keeping those children fed until they're self-sufficient, and dividing your wealth among all your children, neither of which it seems gay uncles help with enough to explain the effect.

But how do we know if this is a valid question - if the situation really needs to be explained at all?

Percentage of the population with the condition. (RichardKennaway's comment explains how you would calculate the 'expected rate' from underlying conditions, but here I'll just use statistical comparisons.)

The rate of major birth defects in the US, as reported by the CDC, is also about 3%.

This comparison is a category error--the comparison isn't "homosexuality" vs. "all birth defects," but "homosexuality" vs. "any individual birth defect." The most common birth defects are in the "1 in 2000" range, not the "1 in 30-50" range; so what the heck is causing there to be ~40-80 times as many homosexuals?

Embryological development is a complex and fragile process, and there are many ways for it to go wrong. We don't wonder how it is possible that selection pressure allows anencephaly to occur in 1 in 4859 births.

Note that anencephaly leads to early death, and you might think that in most evolutionarily relevant time periods, the costs of of raising a child to adulthood may have been significantly larger than the costs in bringing a pregnancy to term. A gene that halves your chance of giving birth to a child with anencephaly will have a very tiny impact on your overall fitness, and thus take a long time to spread through the population.

Obligate male homosexuality greatly harms reproductive fitness.

I'd imagine female homosexuality should have a similar effect.

On the other hand, 'obligate' is a strong word to use for things as complicated as human behavior. Knowing several older male homsexuals with biological children via socially-imposed marriage customs, I don't think the effect is as large as many assume under many environments.

I'd imagine female homosexuality should have a similar effect.

Except that ... how to put this delicately? Historically, men who would prefer not to have sex with women have been more likely to get their way than women who would prefer not to have sex with men.

On the other hand, 'obligate' is a strong word to use for things as complicated as human behavior.

Specifically, there are gay men who are repulsed by the prospect of sex with women, and then gay men who are simply not interested (or not as interested) in sex with women.* It seems to me that 'obligate' is meant to refer to the first cluster, and should have a reproductive penalty roughly the same as male asexuality. (Figuring out what percentage of the population falls into that cluster is hard, since you can't really go off self-reports of preference; you want self-reports of anti-preference.)

*Straight men can consider how they would feel about having sex with another man; for some, there's a visceral disgust reaction, and for some there's just a "but... why would I do that?" reaction or a "eh, any port in a storm" reaction.

Knowing several older male homsexuals with biological children via socially-imposed marriage customs, I don't think the effect is as large as many assume under many environments.

In farming societies where monogamy is the norm and marriages are economic arrangements, it seems to me that the reproductive cost of sexual interest in men is minor (or possibly positive, if men in power are willing to trade resources for sexual favors).

But in societies where polygamy is the norm and men compete for women, it seems likely to me that any man who is less interested in winning is less likely to win, and the costs of sexual interest in men might grow significantly.

In our own society, monogamy is the norm, but marriages are not solely economic arrangements and men do compete for women (and vice versa). If even a small percentage of men does not marry, then it makes sense for men who are not attracted to women to be among them, possibly even reaping some rewards (e.g. two men living together, even if not married, may have a higher than average household income).

Homosexuality has a low heritability, IIRC something like 20% concordance for identical twins. If there was a gay gene you would imagine it would be higher.

Greg Cochrane:

Ulcers are far more heritable than homosexuality, and genetics matters: but you don’t get the ulcers without h. pylori.

Yes, that was one of the reasons I posted this. Wikipedia says even identical twins that share a placenta can differ in sexual orientation, and you don't get more shared-genes-and-environment than that.

Homosexuality is mildly heritable. You can't posit that it's hard for evolution to find a way around it, because it has ways. Perhaps not perfect ways, but the heritability should quickly fall it unmeasurably small values. That really requires explanation. Either there is some hidden benefit (an advantage when expressed in the other sex, avuncular investment, heterozygote advantage) or a recent environmental change (industrial pollution, red queen).

But even if it were not heritable, I think it would still be a big mystery. When you compare it to birth defects, you're comparing one problem against a host of problems. It's worth about the same to evolution to fix the one as to fix all the rest. Yes, the details of brain are more delicate than its mere existence, so you should not be surprised that homosexuality is more common than anencephaly, but it is two orders of magnitude more common.

I wonder why there hasn't been more selection against women having a difficult time giving birth. It's risky, but some women give birth more easily than others, so there's enough variation for evolution to work on.

Part of the reason is probably because of a conflict between the mother, father, and baby. The baby gets all of the benefit of, say, having a bigger head at birth but some of the cost is born by the mother and little by the father so from the baby and father's viewpoint the head size will be bigger than it would be for the mom.

That seems orthogonal to NancyLebovitz's point: some women have lower risk than other women when birthing infants with a given head size.

Also, if a woman dies in childbirth, or even if she's injured enough to not lactate well in the days immediately following birth, that strongly impacts the baby. Evolution may not care about how painful birth is, or even how long it takes (now that we don't need to fear predators), but it certainly cares about risk of injury or death to the mother.

Some gene increases the size of the baby's head at birth raising the baby's eventual IQ by X, but also increases the chance that the mom will die during childbirth by Y. There will exist (X,Y) such that the baby having the gene will increase the expected number of great grandchildren that the dad and baby will have, but decrease the expected number of great grandchildren that the mom will have.

Exactly.

Thanks. I was just going to make that point.

Pelvic structure is in play as well as head size.

Also note that there's more to raising children than lactating. Women typically needed to be in good enough shape to do hunting/gathering/food growing.

See Sarah Hrdy's Mother Nature for a reminder that motherhood takes place in the world, not just between the mother and child.

For obvious political and social reasons, it's hard to be sure how many people are homosexual. Note that we are interested only in obligate homosexuality - bisexuals presumably don't have strongly reduced fitness. The Wikipedia article doesn't really distinguish obligate homosexuality from bi-, pan- and even trans-sexuals. The discussion in the SSC comments used an (unsourced?) range of 1%-3%, which seems at least consistent with other sources, so let's run with that.

Was obligate homosexuality common in the ancestral environment, anyway? If I understand correctly "gays" exist as a recognized social identity only in modern Western societies.
People engaging in homosexual intercourse and relationships probably always existed everywhere, and typically societies with significant influence of Abrahamic religions considered such behavior as a sin and/or a crime while non-Western or pre-Abrahamic Western societies tolerated or even encouraged it, but the general expectation was that people entered heterosexual marriage and had children.

Maybe there is a genetic predisposition to homosexuality but it is unlikely to result in obligate homosexuality, and therefore infertility, outside the specific environment of modern Western societies.

If later-born children are more likely to be homosexual, then it seems trivially true that the more children one is inclined to have, the higher percentage of them will be gay. If any genetic mechanism encourages having more children, we'd expect there to be an apparent genetic link as well.

Alternatively, if error-checking causes spontaneous abortions of homosexual children (assuming homosexuality is an error in construction rather than in the instructions), then we would expect more children to be born to those without that error-checking. (And false positives of whatever error-checking is encoded may make it prohibitively expensive to do so.)

This is a question that needs to be approached mathematically or not at all.

Given a phenotypical property P (supposed binary), currently present in a proportion X of the population, and having heritability H and selective disadvantage D, how will X vary over time, measured in units of a generation?

Solving this mathematical problem requires a mathematical definition of H and D, which I don't have, but this must be standard population genetics. Is there a population geneticist in the house?

One can also add various complications to the model, such as heterozygous advantage, spontaneous mutations that reintroduce P, etc.

The goal is to find a model whose parameters are as accurate as we can estimate them, which is consistent with whatever is known about the prevalence of P now and in the past.