Monthly Archives: January 2017

The Bottom of the Rabbit Hole

female choice

How deep does the rabbit hole go?

Many have asked. There is an answer.

The answer is: the rabbit hole is several hundred million years deep.

Male disadvantage is as old as anisogamous sex itself. Ever since males became distinguished from females, males have been disadvantaged. And that happened not long, in evolutionary terms, after the dawn of multicellular organisms.

If males are privileged, or even if we are equal, where is my uterus?

Feminists promote the view that the possession of a uterus is a burden. Certainly it was when the occupational hazard of being female was a succession of unwanted pregnancies and the curtailment of individual freedom which that imposed. In evolutionary terms, the female invests heavily in reproduction.

By the same token, in evolutionary terms, males might appear to have a lot of catching up to do as regards contribution to the reproductive endeavour. But too naive a view of these matters can lead otherwise sound scientific expositions into a pejorative – even misandric – view of male contribution, such as this quote from Lukas Schärer,

The male sex can be seen as a parasite of the investment by the female sex

Here I take a closer look at these evolutionary matters and opine that the origins of male disposability can be traced all the way back to the origin of maleness itself. I shall suggest that our society’s blasé indifference to male disadvantage is an evolved trait.

The evolutionary purpose of males is to be disposable.

In genetic terms, the male contribution to reproduction, which balances the female’s greater obvious investment, is the high risk of being surplus to requirements – the benefit of which is the eradication of deleterious genes from the species’ gene pool.

Yup, the protection function of males operates even at the genetic level.

The above quote may be turned on its head: the female sex may be seen as parasitic on male disposability – and this is true at great evolutionary depth, not just in human society.

That is the bottom of the rabbit hole.

The account which follows has a fair bit of scientific detail. Just skip the bits you can’t be bothered with.


What is sex for?

No, no, no. If you thought “for having babies” or “for having fun”, go to the bottom of the class. You were thinking of copulation, weren’t you?

Sex is a reproductive strategy defined by the recombination of genes, the offspring sharing genes from two parents. This is usually accomplished by diploid cell meiosis followed by fusion of the resulting haploid gametes to form the new, and unique, first diploid cell of the offspring, the zygote.

[If you are struggling with that last sentence, this para deciphers it. It’s a one para summary of genetic biology: Genes come in packages called chromosomes. (I’ll get to the mitochondrial exception later). Diploid cells involve a set of pairs of chromosomes, one of each pair originating from each parent. Thus, human cells consist of 23 chromosome pairs, 46 chromosomes in all. Meiosis is the process in which such a diploid cell splits in two (in effect, though it’s not so simple) forming cells which each have just one chromosome of each pair. These are the gametes, which are examples of haploid cells (containing single rather than paired chromosomes). The gametes of a female are called eggs, whilst the gametes of a male are called sperm. In humans, 22 of the 23 chromosome pairs are homologous, i.e., each chromosome within a pair, one originating from the mother and one from the father, contain the same genes at the same positions. However, the chromosomes which originate from, say, the father are not the same as the father’s chromosomes (ditto, the mother). This is because during meiosis genetic material from one of the pair of homologous chromosomes ‘crosses-over’ to the other of the pair, thus creating an entirely new combination of alleles in the gametes’ chromosomes. An allele is a particular variant of a given gene, so that allele is to gene as isotope is to element. The 23rd pair are the sex chromosomes which are not homologous, being denoted XX and XY for female and male humans respectively, with Y being physically a relatively small chromosome. Note that this is not universally the case, for example in birds the male is the homomorphic sex (ZZ) and the female heteromorphic (ZW), and Z is the large chromosome. Experts will know that there are a myriad of exceptions to this brief outline, but further details are not appropriate here. Lecture ends.

Apologies if mra-uk seems to be turning into a science blog. I’ll be returning to traditional mra fare after I’ve got this one off my chest.]

Ok, so that is what is meant by sexual reproduction. And sexual reproduction necessarily involves two types of individual in a given species: male and female – right?


So far I have not defined what ‘male’ and ‘female’ mean – and sexual reproduction does not necessarily require sexual dimorphism. If the two gametes which fuse to form the zygote are of comparable size and shape, they are said to be isogamous – in which case the terms ‘male’ and ‘female’ are either undefined or arbitrary or simply do not apply.

Overwhelmingly, plant and animal species are anisogamous: the two gametes are very different in size. The female is defined as the phenotype (individual) which produces the large gamete – the egg. The male is defined as the phenotype which produces the small gamete – the sperm. The sperm is little more than a package of genetic material with a distribution mechanism. The egg, on the other hand, comes complete with the infrastructure and nutrients required ultimately to form a complete diploid cell, the zygote. Eggs tend to be immobile, but sperm mobile. The sperm goes to the egg. This is as true in plants as in animals, wind-blown pollen being the male haploid gametes, the sperm.

The big question is “why”? Why did sex, and in particular anisogamous sex leading to sexually dimorphic individuals, evolve at all? You might think that such a basic question has long been answered. It hasn’t. To quote Paul Cox,

The evolution of anisogamy, one of the major evolutionary riddles to remain unsolved in the nineteenth and twentieth centuries, emerges into the twenty-first century as potent a mystery as ever. The prevalence of anisogamy in the animal and plant kingdoms – with isogamy characterizing only a few algal species – is an astonishing testament of the evolutionary ascendency of anisogamy as a robust evolutionary solution.”

Indeed – but how come?

In truth this modest admission of ignorance belies the great deal that is known about the evolution of sex. Indeed, there are a number of hypotheses which, perhaps between them, probably provide the answer. Before reviewing the possible answers, though, let’s make sure the problem is understood.

Some organisms can reproduce by parthenogenesis, i.e., asexually so that an individual creates offspring without the involvement of any other individual. It is fairly common in lower creatures. The phenomenon will be familiar to anyone who has kept stick insects – their numbers grow alarmingly quickly, despite all being female. Often the offspring are clones of the single parent, but, surprisingly, not always. In automictic parthenogenesis a haploid ovum is first made by meiosis, thus permitting genetic cross-over to occur.

Why would evolution favour sexual reproduction over parthenogenesis? Sexual reproduction produces one offspring for every pair of individuals, whereas parthenogenesis would allow both individuals to reproduce, creating two offspring. This is the two-fold cost of sexual reproduction. Would it not be more efficient, and hence selected for by evolution, to deploy parthenogenesis in all species?

Actually there is an easy way for sexual reproduction to avoid this two-fold evolutionary cost and that is by adopting reproductive hermaphrodites. Each individual could be fertilised by the other, and both would bear children (or lay eggs, as appropriate). So the advantages of genetic mixing between two individuals could be retained but two individuals would produce two offspring, just as for parthenogenesis.

This observation just makes the original question harder. It is now necessary to explain specifically why sexual dimorphism (hence anisogamy) is a successful evolutionary strategy when the male cannot produce a child. In addition to this arithmetical two-fold cost, there is also the disadvantage that dimorphic sexual reproduction requires the male and female to physically find each other (or, at least, their gametes need to do so – think pollen) apparently introducing further inefficiency.

We can phrase this as a radical feminist might: “what use are males?”

Let’s look at some older hypotheses before getting to the main event.

The Tangled Bank

The “tangled bank” is a convenient label for a class of theories stretching back to Darwin (the name originating from a throw-away paragraph of his). Essentially these theories claim that the benefit of sexual reproduction lies in its enhancement of genetic variation, because sex involves the mixing of genes from two parents (in additional to the mixing of genes of each parent via cross-over). I dare say this is what the lay person most commonly believes. The problem with this idea is that it’s wrong. To quote the review, tellingly entitled “Sex reduces genetic variation”, Gorelick & Heng write,

For over a century, the paradigm has been that sex invariably increases genetic variation, despite many renowned biologists asserting that sex decreases most genetic variation. Sex is usually perceived as the source of additive genetic variance that drives eukaryotic evolution vis-à-vis adaptation and Fisher’s fundamental theorem. However, evidence for sex decreasing genetic variation appears in ecology, paleontology, population genetics, and cancer biology.”

Moreover, the theory has some obvious flaws in terms of what it predicts. In Evolution and Human Behavior  John Cartwright writes, referring to the tangled bank hypothesis,

The theory would predict a greater interest in sex among animals that produce lots of small offspring that compete with each other. In fact, sex is invariably associated with organisms that produce a few large offspring, whereas organisms producing small offspring frequently engage in parthenogenesis.”

More helpfully, Gorelick & Heng have this to say,

“…sex acts like a coarse filter, weeding out major changes, such as chromosomal rearrangements (that are almost always deleterious), but letting minor variation, such as changes at the nucleotide or gene level (that are often neutral), flow through the sexual sieve. Sex acts as a constraint on genomic and epigenetic variation, thereby limiting adaptive evolution. The diverse reasons for sex reducing genetic variation (especially at the genome level) and slowing down evolution may provide a sufficient benefit to offset the famed costs of sex.”

Rather than sex increasing genetic variation, it decreases it – but this can be a good thing in terms of getting rid of harmful mutations. However Gorelick & Heng’s optimism that this might provide “a sufficient benefit to offset the famed costs of sex” has not withstood scrutiny. The Tangled Bank does not, on its own, provide a complete explanation of how sexually dimorphic species either evolved or are evolutionarily stable.

The Red Queen Hypothesis

The Red Queen hypothesis recognises that organisms are not in an environment which is static. In particular they are being attacked by parasites which themselves evolve rapidly. There is an arms race between the species and its parasites, both reacting to counter the latest move of the other. So, it takes all the running an organism can do to keep in the same place. More accurately, what is hypothesised is a sort of dynamic equilibrium in which both the species and its parasites evolve at equal rates. In 1993 Matt Ridley published a book on the evolution of sex which he actually titled, “The Red Queen”, so he must have been sold on the idea.

However, it now looks unlikely that The Red Queen hypothesis can be the whole explanation of how anisogamous sex can overcome its two-fold cost. Some studies do indeed produce results consistent with the hypothesis, such as this one. But such results would appear to be specific to particular circumstances, not a general phenomenon. Thus Otto and Nuismer conclude,

The Red Queen hypothesis posits that sex has evolved in response to the shifting adaptive landscape generated by the evolution of interacting species. Previous studies supporting the Red Queen hypothesis have considered a narrow region of parameter space and only a subset of ecological and genetic interactions. Here, we develop a population genetics model that circumscribes a broad array of ecological and genetic interactions among species and derive the first general analytical conditions for the impact of species interactions on the evolution of sex. Our results show that species interactions typically select against sex. We conclude that, although the Red Queen favors sex under certain circumstances, it alone does not account for the ubiquity of sex.”

Recombination as Gene Error / Mutation Purging

We have seen, from Gorelick & Heng quoted above, that sex can act as a coarse filter, removing the more serious genetic defects. For example, Paland and Lynch concluded that their results “support the hypothesis that sexual reproduction plays a prominent role in reducing the mutational burden in populations“. However, the same conclusion does not hold for the gradual accumulation of more minor genetic defects. The hypothesis that sexual reproduction might also purge such accumulations of minor defects is usually associated with the name Alexey Kondrashov. He concludes

If the deleterious mutation rate per genome per generation is greater than 1, then the greater efficiency of selection against these mutations in sexual populations may be responsible for the evolution of sex and related phenomena.”

The trouble is that mutation rates are actually almost certainly smaller than 1 per genome per generation, see for example Estes et al and Keightley and Eyre-Walker. So once again it seems that sex, through recombination and sharing of genes, is not enough to overcome its apparent two-fold cost.

It’s Not Just Recombination

So where does this leave us? It leaves us, as Mary Jane West-Eberhard put it succinctly, with “the paradox of sex, whose maintenance by recombination alone has not been convincingly demonstrated in theory or in fact.”

It would appear that sex itself – which is gene recombination and sharing – does not provide a mechanism sufficient to offset the two-fold cost of sexual dimorphism. So, if it isn’t the sex part, is it the dimorphism part? Does the existence of two distinct phenotypes, the two sexes, provide the mechanism driving sufficient evolutionary benefit?

The answer would appear to be “yes”.

Mary Jane West-Eberhard expresses it thus, “if you concentrate on the social aspects of sex, you can see males and females as two divergent, complementary morphs, mutually dependent alternative phenotypes that are similar to the queens and workers of social insects in their mutual dependence; neither can reproduce without the other.”

So now I turn to explanations based on social behaviour rather than gene recombination and sharing. Whilst these social explanations emerge as being the more significant, it should be borne in mind that recombination does confer benefit – just not enough to offset the two-fold cost of sex, and hence not sufficient to explain the evolution of sex on its own. However the complete explanation of the origin and evolutionary stability of sexual reproduction probably involves both aspects in combination.

Maintenance of Sex Versus Evolution of Sex

Before proceeding, and in the interests of completeness, it is useful to distinguish between two problems: how sexual reproduction evolved, and why it remains stable against further evolutionary changes (“maintenance”). Mary Jane West-Eberhard graphically illustrates the difference thus,

The factors responsible for the functional design of a trait are not necessarily those responsible for its maintenance at high frequency: sports utility vehicles were originally designed for rugged off-road use, but they are maintained at high frequency in many parts of the world for quite different reasons, such as to display signs of wealth and to serve as armored shields against injury in traffic accidents.”

Her view is that sex is maintained as a “developmental trap….a mere legacy of selection past”, hence a phenomenon quite independent of its evolution. She summarises her thesis thus,

Sexual reproduction is maintained as an adaptive legacy of sexually selected and other male manipulations that have produced a reproductive dependence of females on males.”

From this perspective, sexual reproduction is merely a bad habit, long past its ancient evolutionary usefulness. It echoes the earlier quote from Lukas Schärer that “the male sex can be seen as a parasite of the investment by the female sex“.

An analogy of this hypothesis is a non-linear optimisation problem. It is infamously the case that an automated search for the minimum of a function can get stuck in a local minimum which is very different from the global minimum that is wanted. The local minimum is stabilised (maintained) even though it is the wrong solution. Indeed, purely mathematical, game-theoretical, models can ‘explain’ the stability of dimorphic sexual reproduction, see for example Feigel et al’s bullishly titled “Sex Is Always Well Worth Its Two-Fold Cost”. However, it would be an act of faith to assume the assumptions of such models represent reality.

Social Sexual Selection and Mutation Load

And so to the main event. Social sexual selection is beginning to emerge as the mechanism of greatest significance in realising the advantage of sexual reproduction. Mary Jane West-Eberhard expresses it thus,

“(Sexual reproduction has) a ‘eugenic’ function – that is, sexual behavior, such as female assessment of males, is testing for good survival genes. You see female choice and male-male competition as ways of screening for the genetic quality of potential mates in the struggle for survival and ecological success. Agrawal and Siller assigned sexual selection another kind of eugenic function that depicted it as a way of placing the burden of mutation disadvantage on males. By this idea, which we can call “mutational cleansing”, the cost of selection against deleterious mutations falls mainly on the more strongly sexually selected sex, usually the males, and this may help to compensate the cost of sex to females.”

[It should be noted that this is not West-Eberhard’s preferred hypothesis – her views have already been discussed, above – but the quote is useful for its inclusion of the term “mutational cleansing”].

As if in answer to the feminists’ question “what use are men?”, Steve Moxon in Sex Difference Explained From DNA to Society: Purging Gene Copy Errors expresses it thus,

In contrast to females, the job of the males is for their genes to be radically exposed to natural selection, so that those males displaying, relatively, some form of deficiency or less than prowess, through possession of a sub-optimal, below average, or a simply not pre-eminent genome, are identified for weeding out, to take with them their deleterious genetic material, which thereby is eliminated from the local gene pool.”

This overall process, continues Moxon, has been dubbed the male genetic filter by the pioneering biologist and computer engineer Wirt Atmar in his key 1991 paper “On the Role of Males“. Atmar’s key conclusion is,

A primary reason for the existence of males in a bisexual species may be to act as a pre-zygotic filter of genetic defects. Males appear to be an auxiliary sexual caste that may be culled at less cost to the reproductive success of a species than by allowing both maternal and paternal lines of inheritance to be culled uniformly. A variety of genetic and behavioural mechanisms promote and exaggerate a general physiological fragility in male animals not apparent in females.”

Atmar goes on to cite intrasexual male violence as the mechanism by which this culling is achieved. However Moxon has a more nuanced, and more convincing, take on how the culling is achieved, namely through the agency of male hierarchies (addressed briefly below).

Quoting Moxon again,

The extra purging of deleterious material from the gene pool through the male half of the lineage is sufficient to more than compensate for sexual reproduction requiring two parents to make each offspring rather than just the one needed in sexual reproduction.”

To put it simply and brutally, the purpose of males is to be disposable. One might say that the social disposability of men in our society is an echo of its evolutionary, genetic origins.

So much for the statement of the hypothesis that males act as a genetic filter of mutations. What about the evidence? In their 2008 paper, Purging the Genome with Sexual Selection: Reducing Mutation Load through Selection on Males, Whitlock and Agrawal observe that,

Healthy males are likely to have higher mating success than unhealthy males because of differential expression of condition-dependent traits such as mate searching intensity, fighting ability, display vigor, and some types of exaggerated morphological characters. We therefore expect that most new mutations that are deleterious for overall fitness may also be deleterious for male mating success. From this perspective, sexual selection is not limited to influencing those genes directly involved in exaggerated morphological traits but rather affects most, if not all, genes in the genome. If true, sexual selection can be an important force acting to reduce the frequency of deleterious mutations and, as a result, mutation load. We review the literature and find various forms of indirect evidence that sexual selection helps to eliminate deleterious mutations. However, direct evidence is scant, and there are almost no data available to address a key issue: is selection in males stronger than selection in females?

This appears to leave the matter unresolved. However, since 2008 there have been a number of papers which do indeed supply evidence that sexual selection acts more strongly on males. I cannot do a thorough review of the literature in a blog post, even if I had the time and the competence, but a sample of what is emerging is as follows.

Lumley et al, Nature 522, 470–473 (June 2015) write,

Reproduction through sex carries substantial costs, mainly because only half of sexual adults produce offspring. It has been theorized that these costs could be countered if sex allows sexual selection to clear the universal fitness constraint of mutation load. Under sexual selection, competition between (usually) males and mate choice by (usually) females create important intraspecific filters for reproductive success, so that only a subset of males gains paternity. If reproductive success under sexual selection is dependent on individual condition, which is contingent to mutation load, then sexually selected filtering through ‘genic capture’ could offset the costs of sex because it provides genetic benefits to populations. Here we test this theory experimentally by comparing whether populations with histories of strong versus weak sexual selection purge mutation load and resist extinction differently. After evolving replicate populations of the flour beetle Tribolium castaneum for 6 to 7 years under conditions that differed solely in the strengths of sexual selection, we revealed mutation load using inbreeding. Lineages from populations that had previously experienced strong sexual selection were resilient to extinction and maintained fitness under inbreeding, with some families continuing to survive after 20 generations of sib × sib mating. By contrast, lineages derived from populations that experienced weak or non-existent sexual selection showed rapid fitness declines under inbreeding, and all were extinct after generation 10. Multiple mutations across the genome with individually small effects can be difficult to clear, yet sum to a significant fitness load; our findings reveal that sexual selection reduces this load, improving population viability in the face of genetic stress.”

So Lumley et al support the male genetic filter hypothesis. Mallet et al. in BMC Evolutionary Biology 11:156 (May 2011) write,

Sex differences in the magnitude or direction of mutational effect may be important to a variety of population processes, shaping the mutation load and affecting the cost of sex itself…..Mutation-accumulation (MA) experiments provide the most direct way to examine the consequences of new mutations…..We therefore investigated the effects of 50 generations of X-chromosome mutation accumulation on the fitness of males and females derived from an outbred population of Drosophila melanogaster. Results: Fitness declined rapidly in both sexes as a result of MA, but adult males showed markedly greater fitness loss relative to their controls compared to females expressing identical genotypes…..Conclusions: Our data helps fill a gap in our understanding of the consequences of sexual selection for genetic load, and suggests that stronger selection on males may indeed purge deleterious mutations affecting female fitness.”

Again this is supportive of the male genetic filter hypothesis, as is the paper Differential selection between the sexes and selection for sex by Roze and Otto, Evolution 66(2):558-74 (February 2012), extracts from whose Abstract are,

Anisogamy is known to generate an important cost for sexual reproduction (the famous “twofold cost of sex”). However, male-female differences may have other consequences on the evolution of sex, due to the fact that selective pressures may differ among the sexes….it has been suggested repeatedly that sexual selection among males may help to purge the mutation load, providing an advantage to sexual females. However, no analytical model has computed the strength of selection acting on a modifier gene affecting the frequency of sexual reproduction when selection differs between the sexes. In this article, we analyze a two-locus model using two approaches…..We find that costly sex can be maintained when selection is stronger in males than in females, but acts in the same direction in both. Complete asexuality, however, evolves under any other form of selection.”

Further support for the hypothesis is provided by McGuigan et al, Reducing mutation load through sexual selection on males, in Evolution 65(10):2816-29 (October 2011), and by Maclellan et al, Sexual selection against deleterious mutations via variable male search success, Biol Lett. 23;5(6):795-7 (December 2009). However, it would be wrong to give the impression that this view is unanimous – or even that there is, as yet, a consensus. For example, in July 2012, Arbuthnott and Rundle, Evolution 66(7):2127-37,come to the opposite conclusion in a paper whose title is indicative: Sexual selection is ineffectual or inhibits the purging of deleterious mutations in Drosophila melanogaster.

My amateur impression is that the male genetic filter idea is certainly respectable, and probably currently the lead contender as an explanation of the net benefit of anisogamous sexual reproduction despite its famous two-fold cost. However, there does not have to be a single mechanism which provides the entire benefit. It is clear that recombination effects alone do provide some of the benefit. There are, though, two further strands to the argument in favour of the male genetic filter hypothesis: preferred male gene expression and the ancient breeding ratio, which we look at next.

Preferred Male Gene Expression

The purging of gene errors through the preferred culling (or childlessness) of males is of benefit to the species as a whole, both males and females. This would be the case even if genes originating from both parents were expressed equally. But another emerging fact appears to be that more of an offspring’s genes originating from the male are expressed than those of female origin. (“Expression” in this context refers to the allele of the homologous gene pair which is actually “used”, i.e., has an effect on the phenotype, the individual). This will make the male genetic filter mechanism even more effective.

One feels for the radical feminist. The thought that half their genetic material, the very stuff of their bodies, derives from a man must be disgusting to them. Well, in terms of expression, it’s actually rather more than half.

The key paper is Crowley, et al, Nature Genetics 47, 353–360 (2015). Their work was on mice, but they have reason to expect it to be applicable to humans. Their main finding was, “a new global allelic imbalance in expression favoring the paternal allele”. Despite some technical language, the reader will grasp the import of the following extracts from the paper,

Imprinted genes were 1.5 times more likely to be expressed from the paternal than the maternal allele. This observation is consistent with the observation that paternal expression predominates in brain, while maternal expression predominates in placenta. To test whether this asymmetry in parent-of-origin effects extends beyond imprinted genes, we estimated the parent-of-origin effect in each cross and each sex separately. We found that 54–60% of genes show higher expression from the paternal allele, significantly different from the expectation of 50%…..Among the 19 autosomes, 15 have a higher proportion of genes whose neighbor has the same parental skew than expected by chance.

We can calculate a rough estimate of the number of genes with paternal over-expression, simply by taking the difference between the number of genes with higher paternal minus higher maternal expression. For example, for female CAST/EiJ × PWK/PhJ reciprocal hybrids, there are 1,652 more genes with allelic imbalance in favor of the paternal allele (6,790 paternal minus 5,138 maternal over-expressed genes)…..the excess of genes with paternal over-expression ranges between 938 and 2,500…..However, this likely represents an underestimate because, while we have high power to identify classical imprinting, we lack sufficient power to identify all genes with modest parental overexpression, while correcting for multiple testing.”

To emphasise the import of this, Moxon, quoting one of the authors of Crowley et al (2015) writes,

We now know that mammals express more genetic variance from the father. So imagine that a certain kind of mutation is bad. If inherited from the mother, the gene wouldn’t be expressed as much as it would be if it were inherited from the father.”

In other words, it’s more important to get good genes from the male, so evolutionary pressure acts more severely on the male. The excess of male genes which are expressed amplifies the male genetic filter mechanism of gene mutation purging.

In another 2015 paper, Sexual selection drives evolution and rapid turnover of male gene expression, Proc Natl Acad Sci U S A.112(14):4393-8, Harrison et al note the “profound and pervasive differences in gene expression observed between males and females“.

Ancient Breeding Ratio

Finally a piece of evidence which might be the smoking gun. There is reason to believe that, if you could compile a list of all your ancestors going back 50,000 or 100,000 years, twice as many of them would be women as men. This remarkable conclusion is often expressed in this form: on average since ancient times, about 80% of women bore children, but only about 40% of men had progeny. Clearly, if true, this supports the hypothesis of a male genetic filter in which only the fitter portion (~40%) of every male cohort gets to breed. Sexual selection, by female choice and male dominance – or perhaps premature death – prevents lesser men reproducing at all.

This remarkable conclusion originates from genetic studies reported in 2004 by Wilder et al, Mol Biol Evol 21 (11): 2047-2057, Genetic Evidence for Unequal Effective Population Sizes of Human Females and Males. It is, obviously, indirect. The paper analyses gene sequence variances in local populations. By concentrating on the non-recombining part of the Y-chromosome DNA, genetic variance generated by the male line only is determined. Similarly, by concentrating on mitochondrial DNA, genetic variance generated by the female line only is determined. (Mitochondrial DNA does not reside in the chromosomes and is inherited from the mother alone). If genetic changes occur at some fixed rate per generation, then genetic variance provides a means of gauging the time to the most recent common ancestor (TMRCA).

But it turns out that the mitochondrial DNA variance is double that for non-recombining Y-chromosome DNA. This seems to suggest that the TMRCA for males is only half that for females – which makes no sense. But actually it is not calendar years which matters, it is the number of individuals contributing to the breeding process. Wilder et al conclude that the effective male breeding population, averaged over ancient times, was only half that for females.

A potential alternative explanation for the differing male-female genetic variances was suggested, namely the far higher rate of female migration due to the cultural practice of patrilocality (or exogamy) in which it is the woman who moves to live with her husband’s family upon marriage. However, this was addressed by another paper from Wilder et al, Nature Genetics 36, 1122 – 1125 (2004), whose title is all you need to know: Global patterns of human mitochondrial DNA and Y-chromosome structure are not influenced by higher migration rates of females versus males.

Similar studies have been carried out since 2004 but without essential contradiction, as far as I am aware. It would be interesting to examine the historical evidence for (or against) the idea that 80% of women but only 40% of men had progeny (though do note that the DNA evidence relates mostly to prehistory). Matt Ridley, in ‘s The Red Queen, attributes the following view to Laura Betzig,

“(In medieval Christendom) the phenomenon of monogamous marriage and polygamous mating was so entrenched that it required some disintering. Polygamy became more secret, but it did not expire. In medieval times, the census shows a sex ratio in the countryside that was heavily male-biased because so many women were ’employed’ in the castles and monastries. Their jobs were those of serving maids of various kinds but they formed a loose sort of ‘harem’, whose size depended clearly on the wealth and power of the castle’s owner. In some cases, historians and authors were more or less explicit in admitting that castles contained ‘gynoeciums’, where lived the owner’s harem in secluded luxury.”

Ridley adds, “Meanwhile, many medieval peasant men were lucky to marry before middle age and had few opportunities for fornication” and “A feudal vassal’s son had a good chance of remaining childless, while his sister was carried off to the local castle to be the fecund concubine of the resident lord“.

I cannot vouch for the historical accuracy of this view, though it does conveniently align with the (ancient) DNA evidence. It would be interesting to make a more detailed study.

In passing I cannot resist addressing a spurious claim that has been touted around the popular press, namely that the Y-chromosome is shrinking and destined to disappear. It is remarkable the variety of forms which misandry can take – or perhaps it is just wishful thinking by the radicals. Anyway, it is not so. The findings of Rozen et al, Am J Hum Genet. 85(6): 923–928 (December 2009), are “at odds with prominent accounts of the human Y chromosome’s imminent demise“. In any case the geneticists who were the source of this misinformation were ‘predicting’ the Y-chromosome’s demise only in 10 million years, not a timeframe which causes me much unease. But even that is incorrect, being based on Y-chromosome gene loss which occurred tens of millions of years ago. In contrast, I quote,

During the 6,000,000 years since divergence of the chimpanzee and human lineages, the chimpanzee Y chromosome has lost the function of four X-degenerate genes, possibly as a result of increased specialization for spermatogenesis. By contrast, the human Y chromosome has not lost any X-degenerate genes during the same 6,000,000 years. Our present findings show that, in addition, X-degenerate gene content in the overwhelming majority of human Y lineages has changed little since the last common ancestor of modern human Y chromosomes, ~100,000 years ago. Indeed, the results reported here imply that purifying selection has been effective in stabilizing and maintaining the amino acid sequences of the human MSY’s X-degenerate proteins during this period. In combination with previous studies, our findings conclusively refute models of precipitous genetic decay in human Y-chromosome lineages.”

The Male Hierarchy

The male genetic filter mechanism can only work if males with ‘good genes’ mate preferentially. But how is sexual selection to accomplish this preference for males with ‘good genes’? Females choose, but females must also be able to distinguish between males with ‘good’ and ‘poor’ genes. In birds this is often achieved through the bright plumage of male birds, the peacock being the ultimate example. And in some cases pure physicality makes the matter unambiguous: he mates who is the one left standing after a fight.

But in humans the matter is more complex. There are many male hierarchies. Being physically imposing is just one, and one of the least significant: these days powerful men rarely have bulging muscles. Wealth and social status are the chief determinants of the male hierarchy in human societies, and these are virtually independent of physique – for men, that is. Female hypergamy is the male genetic filter in action.

It is worth noting that there was a long standing dispute about whether female choice need actually be correlated with “goodness” of the male’s genes, in any objective sense. A point of view normally associated with Ronald Fisher is that any ‘fashion’ amongst females for a particular male characteristic can become self-sustaining. (If a female bucks the fashion trend she is likely to have a male offspring who is unfashionable, and hence who is less likely to mate). However, the male genetic filter hypothesis requires that female choice really is correlated with genetic quality in the male – or, rather, that the de-selected males are those in whom the genetic defects are concentrated and ripe for purging.

The purpose of the male hierarchy (or hierarchies) is to provide the female with a ready-made ranking which, the hypothesis claims, is correlated with genuine genetic quality. Such a linear hierarchy is achieved through transitive pair-wise ordering, as explained by Moxon, who writes,

Dominance is adaptive stressing and ranking of males in the service of allocating reproduction by differential self-suppressed fertility

The male dominance hierarchy is therefore the perfect tool for implementing the male genetic filter.

In pair-wise conflicts or assessments, only males behave in a manner which takes account of previous outcomes so as to form a linear dominance hierarchy. Moxon  opines that such dominance hierarchies are unique to males because the neural functionality which supports the formation of such a hierarchy is specific to the SRY gene on the Y-chromosome (see van den Berg et al).

I will not attempt to address female hierarchies except to note that they will inevitably be of a different kind from male hierarchies if the male genetic filter hypothesis is correct (see Moxon). Men seek power to gain access to sex, women seek sex to gain access to power.

For men, ranking exacerbates conflict, writes Moxon, because it’s worth fighting for. Hence ranking based on violence is unnecessary, and actually undesirable, in females because injury is best avoided and there is nothing to gain by taking the risk. This explains why most violence is male-on-male, since its purpose is to establish the male hierarchy. Male-on-female violence is an aberration because it risks injury to the limiting factor in reproduction (the female) and hence is counter-evolutionary, which is why it is socially prohibited. Female-on-male violence is neutral in evolutionary terms and is probably an epiphenomenon of female control of the male via the pair bond. However, both directions of inter-sex violence are untypical.

If the male genetic filter hypothesis is correct, male violence, and in fact all forms of male competitiveness, are ultimately for the benefit of the whole species, and females in particular since they are spared being the chief sacrifice.

Male Culling

Failing to be sufficiently high in the male hierarchy can lead to a man failing to reproduce. However there is another way in which the male genetic filter can operate: by premature death. Seager, Farrell and Barry remind us of the greater health risk to males, including as a foetus or young child before lifestyle issues become relevant,

In a British Medical Journal article called ‘The fragile male’, the many ways in which men are biologically more vulnerable than women are highlighted. The male foetus is at greater risk than the female of virtually all medical complications (e.g. cerebral palsy) and developmental disorders (e.g. autism). Perhaps it is the height of irony then for males unthinkingly to be expected to be the more resilient sex, showing that sex and gender differences operate from the moment of conception and in some unexpected ways the differences favour the female.”

Perhaps not irony. Perhaps an evolved strategy to place extra survival pressures on males as part of the male genetic filter? The conclusions of the BMJ article read almost like something from a men’s rights blog (well, they do now),

The disadvantages of the male are usually seen as socially mediated. Even from conception, before social effects come into play, males are more vulnerable than females. Social attitudes about the resilience of boys compound the biological deficit. Male mortality is greater than female mortality throughout life. The causes are a mixture of biological and social pressures: we need to be aware of both in order to promote better development and health for boys and men.”

A couple of extracts from Matt Ridley’s The Red Queen refer to the hormonal component of greater male vulnerability to disease,

There seems to be something about steroid hormones that unavoidably depresses the immune defence. This immune effect of testosterone is the reason that men are more susceptible to infectious diseases than women, a trend that occurs throughout the animal kingdom. Eunuchs live longer than other men, and male creatures generally suffer from higher mortality.

(And, quoting Zuk) Males are thus necessarily more vulnerable to disease as they acquire the accoutrements of maleness.”

At birth, in the UK, male babies outnumber female babies, the sex ratio at birth being 1.054, so that 51.3% of newborn babies are male and 48.7% are female. And yet, in the population as a whole, only ~49% of people are male and ~51% are female – as our Chief Medical Officer, Dame Sally Davies, seems to take delight in reminding us. This turn around occurs because, before the age of 84, there are ~37,000 more deaths of males than females per year. Moreover, the excess of male over female deaths occurs in every age range, from tiny babies to age 84. And the percentage excess of male over female deaths is not just one or two percent, but several tens of percent in every age range – typically about 50% more male deaths. (See here for the data).

The top two causes of the excess premature male deaths are cardiovascular diseases and cancers (see here). This may be related to lifestyle issues, and that is certainly the case for the third and fourth in the list of excess male deaths: drug and alcohol abuse and suicide. So it’s men’s own fault then, is it? Or is the tendency of men to adopt riskier behaviours all part of their evolutionary inheritance? Are these excess male deaths actually one of the enactments of the male genetic filter – culling of the less worthy or the medically weaker?

Then there are deaths in war (almost ~99% male), deaths at work (~98% men), deaths of rough sleepers (~88% men). And there is the irritating negligence of men when it comes to looking after themselves medically. Indeed, we might ask whether the entire male gender script (be a fighter and a winner, be a provider and a protector, retain mastery and control over your feelings) is actually an enactment in the social sphere of the male genetic filter – with the added bonus that these behaviours are also beneficial to the rest of society?

Perhaps the most convincing evidence that this is all an evolved strategy is the fact which exercises men’s rights activists the most: that despite the litany of male disadvantages, virtually no one cares. It is almost as if acceptance of male disadvantage, even fatal disadvantage, is an inherent trait in Homo sapiens, isn’t it?


Well, at the very least I hope I have given the lie to the sentiment that “the male sex is  parasitic on the investment in reproduction by the female sex”. This may be refuted even without invoking the not-insignificant issue of resource provisioning. The male genetic filter is a high price paid by men-as-a-class to maintain the genetic integrity of the species. It appears that more than half of men in antiquity had not the opportunity to be parasitic upon women’s reproductive investment. To reiterate my starting claims,

The evolutionary purpose of males is to be disposable.

In genetic terms, the male contribution to reproduction, which balances the female’s greater obvious investment, is the high risk of being surplus to requirements.

Patriarchy, you will note, can have no relevance to a man not within a family.

But are present day social disadvantages of men and boys truly to be seen as a consequence of this ancient biological weregild? Or is it mere analogy or poetic echo?  The answer, I think, is that female choice and male hierarchies are still very much in place. Is the collapse of marriage in the lower socioeconomic classes the result of the male genetic filter?

Whether the male genetic filter is still effective in purging poor genes is another matter. Probably this has been defeated by the welfare state which undermines a woman’s previous disinclination to become pregnant by a low-ranked male.

It is reasonable to suppose that the male hierarchy / female choice mechanism would be implemented, in a species with high cognitive function, via evolved sex-dependent psychologies. Since males are, in effect, seeking female approval, this naturally leads to male deference towards females but a critical attitude of females towards males. It also naturally gives rise to intra-male competition (as opposed to cooperation). In fact, Moxon argues, the critical view of men will extend to men themselves, as a means of policing any tendency an individual may have to cheat and “dishonestly signal” his status on the hierarchy. Indeed, policing the honest operation of the male hierarchy is stressed as central by Moxon.

Inevitably, then, men are judged by harsher standards than women, because the judging of men is a key evolutionary requirement, whereas judging women is not – beyond, of course, indicators of youth and health, the correlates of fertility. Moxon writes,

That, in root biology, males are obliged to mutually contest in order to earn sexual access, is bound to have major ramifications in psychological and social terms: males are seen as having to earn regard, otherwise they are presumed to be worthless….. Women would have to behave conspicuously badly to earn disapproval from males; otherwise, invariably they are well regarded…..All kinds of normal behaviour by males may be tendentiously interpreted as actually or potentially ‘anti-social’ in some way, and males come to be held responsible – blamed – for their own policing.”

John Gray reminds us that we are animals and any inclination to regard ourselves as having risen above our animal natures is conceit and self delusion. If the male hierarchy / female choice mechanism is an inherited psychological trait, it will not be easily ignored. And in as far as traditional pair bonding habits have been socially discouraged, so the male hierarchy / female choice tendency must manifest in other forms. Women are now discouraged from reliance upon males and their ‘privilege’ hierarchy. So how is their innate tendency to judge males based on their hierarchical rank to find expression? Is this the psychological origin of much of the misandry? Is the anti-lad culture on campuses, the rise of ‘misogyny’ hate crimes, and the myriad of man-shaming tactics actually a subconscious attempt by women to exercise their evolved ‘right’ to criticise men – but now stripped of any positive connotations, divorced from its original purpose of examining male rank for the purposes of reproduction?