Are Males the main evolutionary tool for production of genetic variation necessary for evolution?

Question

What I'm saying here is just a personal reflection, that might turn to be gravely erroneous, actually I'm asking that because I didn't see it presented elsewhere.

Evolution is propelled by two directions. The first one is a process that is novel in producing genetic variation, which includes: Mutation and Migration. The second is a clearing up process, something that wash out results from the first process, and those are: Natural Selection and Genetic drift.

Natural selection is more functional in the sense that it only preserves traits that are adaptive to the environment. Genetic drift is not discriminating in that sense, so it can wash out any result of process 1 whether its harmful or beneficial.

It's clear that the primary source of evolution is the first process (i.e.; mutation and genetic migration), since the second process (i.e.; natural selection and drift) only acts on what results form it.

[Note: by primary "source" of evolution, its meant here to be what's responsible for producing the basic material upon which evolution works, since evolution is change in genetic variation over generations, then "genetic variation" is the basic material for evolution, and this is produced by mutation and migration. Natural selection and drift don't produce genetic variation, they change it by an act to decrease it, and a process that acts to decrease something, can hardly be viewed as a producer of that thing. A butcher is not the primary "source" of meat, the cow is!]

Now in principle the more we have production of genetic material the more is the chance of getting a genetic change that is useful. Of course increase in mutation rates can result in injurious traits, those would be washed out by selection and drift, however its the higher probability of having a beneficial mutation that is the primary concern here.

The male spermatogenesis in mammals supplies the impression that it is the MALE sex that is the Ore of evolution. The incomparably high cell production rate of all stages of spermatogenesis as compared to Oogenesis, tends to make one think that the chance of mutation arising in spermatogenesis is ought to be much higher than that arising in Oogenesis.

The testis seems to be the Oven in which genetic variation is baked. The rapid turnover of spermatogenesis, whereby each primary spermatocyte finally results in 4 sperms (Compared to One Ovum resulting from each primary Oogonia), that's beside the very large number of sperms produced daily, that continues for years and year. While with the Oogenesis everything really finishes at the foetal life, the remaining is just maturation steps, nothing is new as far as change of genetic material inside the Oocytes is concerned, this is the state throughout most of the female's life.

When I look at the seminiferous tubules, and see all those layers of spermatocytes leading to sperms, I tend to think that there is even some small scale natural selection, that bad mutated germline cells would die off, and only the ones with good genomes would survive all the stages of spermatogensis, and possibly the ones with beneficial mutation might have an advantage in survival in that milieu and even might have better chances of fertilizing the ovum?

Not only that, the testis seems to be more exposed to stressors inside the body and even to direct external environmental stressors, while the Ovaries lying deep inside, seem to be more protected. The Oocyte actually "selects" one sperm, so it's rule is selective rather than productive of change.

All of that makes one think that it is the male germline cells that could mediate high mutation rate in response to stressors, or even without stressors by virtue of the very high production rate of germline cells for very long periods of time. It seems that this is the real source of beneficial mutations that would ultimately drive evolution.

Four connected questions:

1. Is the mutation rate in male germline higher than in female germline?

2. If Yes, then doesn't this mean that Males are more likely the source of most beneficial genetic mutations, which is the main drive for evolution?

3. If 1 and 2 are true, then are we justified in inferring that "being the main source of beneficial genetic mutations" is the main purpose behind evolution of a Male sex?

4. Was this idea proposed before?

Answer 1

1. Yes. The rate of de novo mutations has been found to be higher in paternally derived DNA from several papers. A recent paper from a quick search [1] found that ~80% of 15,746 de novo mutations in 225 families were paternally derived.

2. Based on the total mutations yes, but they are also even more likely to bring deleterious mutations. So per base probably not.

3. That doesn't make much sense. Consider a lowly prokaryote organism that replicates asexually. The replication process is not much different than spermatogenesis. So it doesn't explain why sex differentiation occurs. More likely sex differentiation occured to promote genetic diversity (by preventing self-replication) and rather than the male sex evolving towards increased gamete replication, the female sex evolved towards decreased gamete replication due to selection against pregnancy at older ages (when the body is more fragile and sensitive to giving birth). This is just my speculation I have no references.

4. Yes. It's called Male-Driven Evolution. [2].

[1] Parental influence on human germline de novo mutations in 1,548 trios from Iceland. Jonsson, H, et al. 2017

[2] The rate of spontaneous mutation of a human gene. Haldene, J.B.S.1935

Answer 2

If I actually understand your premises, which is a big if, you're asking if the genetic material in the sperm has been subjected to more mutation than its counterpart in the egg... by the time of mating. In case of humans, where's there's a lot of research and the answer is almost certainly yes.

Recent [GWAS] studies have shown that 76% of new mutations originate in the paternal lineage and provide unequivocal evidence for an increase in mutation with paternal age.

The general theory how this works (which you seem to repeat) goes back to...

Haldane (1947) suggested the following general mechanism for the sex differences in mutation rate: “The primordial oocytes are mostly if not all formed at birth, whereas spermatogonia go on dividing throughout the sexual life of a male. So if mutation is due to faulty copying of genes at a nuclear division, we might expect it to be commoner in males than females.”

As for [your] choice of terminology...

Subsequent estimates of a higher mutation rate in males from molecular genetic data led Miyata et al. (1987) to suggest that evolution is “male‐driven.”

And a more contemporary term is male-biased mutation:

The concept of male-biased mutation has been thoroughly analysed in recent years using an evolutionary approach, in which sequence divergence of autosomes and/or sex chromosomes are compared to allow inference about the relative contribution of mothers and fathers in the accumulation of mutations. For instance, assuming that a neutral sequence is analysed, that rate heterogeneity owing to other factors is cancelled out by the investigation of many loci and that the effect of ancestral polymorphism is properly taken into account, the male-to-female mutation rate ratio, am, can be solved from the observed difference in rate of X and Y chromosome divergence. The male mutation bias is positively correlated with the relative excess of cell divisions in the male compared to the female germ line, as evidenced by a generation time effect: in mammals, am is estimated at approximately 4–6 in primates, approximately 3 in carnivores and approximately 2 in small rodents.

Finally one needs to be careful what one means by variation because...

The creation of genetic variation by recombination can be a much faster process than its creation by mutation.

If we could somehow turn off mutation, in a large population meiotic recombination would still result in new combinations in offspring for quite a while. Eventually, after this combinatorial space is exhausted, we'd only see organisms that repeat something that is already living or has lived in the past.

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So, I've dealt with your 1 & 4. As for theories why we see this male-bias in mutation... (your 2-3) it gets more complicated:

A general theoretical perspective is that level of mutation is a balance between deleterious mutations reducing fitness, advantageous mutations increasing fitness, and cost in fitness from mutation repair mechanisms to reduce the mutation rate (Sniegowski et al. 2000). The relative importance of these factors may vary but because most mutations are generally less fit than the present wild type, selection generally should act to reduce the mutation rate by improving the repair mechanisms. However, the strength of indirect selection changing the mutation rate, either increasing it or decreasing it, is quite low and is on the order of the change in the mutation rate caused by a modifier locus (Sniegowski et al. 2000).

Using the context above, sex differences could be the evolutionary result of selection for a more efficient lowering of the detrimental mutation rate in females, a retention of a higher advantageous mutation rate in males, less cost for lowering the mutation rate in females, or a combination of these factors. One evolutionary hypothesis for sex differences in mutation rates is that there may be different selective optima in the two sexes balancing the deleterious mutation rate and the cost of efficient repair and replication (Ellegren 2007). More specifically, if we assume that the major impact of selection on mutation rate is to minimize the mutation rate per replication as much as possible to reduce rate of deleterious mutation, then any sex differences observed in mutation rate may be related to the different number of replications in the two sexes. In other words, if the major impact of selection is to reduce mutation rate as much as possible, it has been generally more successful in females, either because of more male replications or because repair mechanisms are more efficient in females than males for some reason. Consistent with this, Crow (2000) suggests that an increase in mutation rate at later reproductive ages is not surprising. His reasoning is that until recent times few men would live into their forties so there would have been little selection pressure to reduce the detrimental effects of mutations from older men. Or, the sex differences in mutation rate may not have a strong evolutionary basis and are primarily the result of sex differences in gametogenesis.

As you can see, like most theories regarding the evolutionary reason for some mechanism that itself affects evolution... it's not settled science.

So, regarding 2-3. I think I get your point that if we pick a mutation that has survived until today, there's higher chance it came from a male (2). Even if this is true, it implies little about the evolution of sex-bias in mutation.

You infer (3) that

"being the main source of beneficial genetic mutations" is the main purpose behind evolution of a Male sex

I think the discussion is getting more into philosophy than science at this point. As previous long quote says, it could simply be that natural selection was bad at reducing something that is, on-average, detrimental, but was worse at reducing it one group, i.e. in males, e.g. because it's harder to reduce there. So, assuming that's the case, the "main purpose" of evolution could have been this reduction, and the fact that beneficial mutations (like all mutations) are more often traced to males, is just a statistical artifact of the (mutation reductive) "main purpose".