Did males start as parasites?

Many years ago I was curious about why sexual reproduction is so prevalent. This is a summary of what I found when I investigated.

There is a standard theory to explain sexual reproduction, but it only answers half the question. The standard theory is that a species with sexual reproduction has a pool of genetic diversity. Should the environment change suddenly (temperature changes, a new disease, more effective predators arrive, etc), any gene that helps will have an improved chance of survival and will quickly spread through the population. Without sexual reproduction any particular gene line would eventually go extinct unless it was lucky enough to have the beneficial mutation happen within it. Therefore sexual reproduction allows for much faster adaptation, and benefits the species that does it.

This is all well and good, and convinces me that sexual reproduction has advantages asexual reproduction (as well as being more fun), but it doesn't explain why we have distinct sexes. For instance look at the lowly earthworm. They are hermaphrodites. When they meet they impregnate each other, and both go off and have babies. Hermaphrodites therefore reproduce twice as quickly as a male/female version would. Why, then, aren't we all hermaphrodites?

It can't be a simple quirk of genetics. The genetics of sex reproduction is much more plastic than most people realize. Even if we stick to vertebrates you can find strange things such as hermaphrodites (mangrove killifish) and animals that change gender (African reed frogs, several kinds of fish). So gender is more complicated than the familiar XX vs XY rule for mammals that we learn in biology. If hermaphroditic reproduction was evolutionarily favored, there are enough ways to get there that you'd expect it to be more common than it is.

As it happens I have never encountered a biology text that attempts to tackle this part of the question. However many years ago I came up with a theory that seems reasonable to me. I've discussed this theory with a number of biologists who agree that it seems probable to them as well. So this is my theory, but it is at least plausible. And for all I know it is the standard theory in evolutionary biology, and I just never encountered any source that presented it. (I'm very much not a biologist.)

My theory is that males started as parasites. More precisely, cheaters in a sea of hermaphrodites. And once men were effective enough, the ability of hermaphrodites to impregnate each other atrophied and you got strict sexes.

Let me break this down in more detail.

Imagine a population of hermaphrodites. Now add individuals who can impregnate others, but can't themselves be impregnated. These are males. By refusing the be impregnated the males avoid the hardest part of reproduction. This gives them more energy to devote to impregnating others. As long as the cheater impregnates hermaphrodites twice as fast as hermaphrodites do, this strategy works out.

Evolutionary theory has studied cheating strategies like this. Theory says that in any given environment there will be a natural fraction of the population that is male. With more hermaphrodites/male than the ideal, the male strategy becomes more effective, so the male population will rise. With too few hermaphrodites/male the male strategy becomes less effective so the male population falls. The ideal mix is called the evolutionarily stable strategy. (For another example of an ESS, some salmon fight for the right to spawn, and some try to sneak in while spawning is happening. We can calculate the ideal ratio between how many males should try to fight vs cheat, and it is very close to the actual measured ratios in real salmon.)

If your imagination fails you, don't worry. This isn't a hypothetical possibility, we can find this exact kind of mix of hermaphrodites and males (with no females) in c. elegans. That is a nematode that a lot of biologists study. (Biologists often like to work with organisms that are heavily studied for the simple reason that when they need to know something tangential to their research about how that organism works, there is a good chance that someone else has already studied it.)

In this situation males are cheaters. Biologically in some ways they parallel a virus - they are unable to reproduce on their own but can reproduce by hijacking the reproductive system of their hosts. However biologists have found that symbiosis arises easily out of parasitic relationships. And that is what I believe happened with the genders.

Take our previous population. Imagine that the males are numerous and effective at their job. So effective that a hermaphrodite who attempts to find another hermaphrodite to impregnate will expend so much energy that she would have more children if she just let herself be impregnated more frequently by the very convenient males. In this situation a true female strategy makes sense. And once hermaphrodites take that step, it is only a question of time before the ability for a reproductive individual to play both the male and female parts atrophies, and strict genders emerge.

For more interesting thoughts on sexual differences in humans, here is a psychologist discussing the consequences of men being expendable. I don't agree with all of his conclusions, but he is starting with solid facts that most people aren't aware of. For instance here is confirmation that men are significantly over-represented both at the top and bottom of a lot of distributions.

And in a very different vein, I have long liked David Brin's Neoteny and Two-Way Sexual Selection in Human Evolution. A summary can't do it justice. It comes up with a plausible theory explaining topics as diverse as why women have breasts to why so many men are pedophiles. Even if, no especially if you think that it has to be BS, it is worth the read.