Note: I've edited the post to swap explanations #5 and #6, and added new counterarguments against the importance of #5 (self-fertilisation).

There are many explanations of the evolutionary value of sex in terms of gene exchange (I particularly like this one). But these don’t explain the evolutionary value of having sexes: of the differentiation between males and females. A species of hermaphrodites would get all the genetic benefits of sex, but without the massive cost of half its population being unable to bear offspring. On average, each individual could have twice as many offspring, unless other problems arose. And indeed, most plants are hermaphroditic - but only a few animals. So why aren’t most animals hermaphrodites? A quick search doesn’t turn up any widely accepted answer, so I’ve brainstormed a few possibilities. I may well be missing something obvious; if so, let me know.

  1. Resource cost of being hermaphroditic. If there’s a strong division of labour between males and females, then maybe it’s harder for hermaphrodites to gather enough resources to support offspring. But in many species the males contribute little in terms of resources - e.g. in orang-utans, who are very solitary.
  2. Developmental or metabolic costs of being hermaphroditic. Maybe it’s just a very expensive adaptation. But this seems unlikely to be the main factor - the relevant baseline is the existence of males at all, which is a huge energy cost.
  3. Difficulty of evolving hermaphroditism. Maybe this is just hard for evolution to find? But non-reproductive hermaphroditism seems like it arises via mutations pretty frequently, so I’d be surprised if reproductive hermaphroditism were unachievable by evolution. And in fact there are a few hermaphroditic species - so why haven’t they spread much more widely?
  4. Difficulty of fixating hermaphroditism. A hermaphrodite in a species without many hermaphrodites is likely not as attractive to females as most males are, nor as fertile as most females are. So maybe, even after arising, the trait will be selected against. But on timeframes where sexual desires can themselves evolve, all else equal we should expect stabilising sexual selection towards the best combination of fertility and attractiveness. E.g. it would be undesirable to be impregnated by overly masculine conspecifics, because the resulting offspring would be less fertile themselves. So this adds a bit more difficulty to reaching the hermaphroditic equilibrium, but doesn’t answer the core question of why that’s a less fit equilibrium.
  5. Self-fertilisation. I remember reading a while back that self-fertilisation has a strong short-term advantage, despite losing out on the long-term benefits of sex (this old paper has a section on “selection in favour of self-fertilisation”, although I haven’t read it in detail). So maybe the answer is that hermaphrodites end up evolving ways to self-fertilise, which is harmful in the long run, and so group selection prevents the trait from becoming too widespread. This effect plausibly occurs in plants, but not strongly enough to prevent most of them from being hermaphroditic. And presumably it's significantly harder for plants to prevent self-fertilisation (since their pollen spreads widely) than it is for animals.

I’m open-minded to the possibility that a combination of these explanations is responsible. But none of them seems particularly strong to me; so I'm guessing that the biggest effect comes from:

6. Physical dominance. Maybe animal competition to impregnate fertile conspecifics is grounded in physical power, so that dominant males could just prevent hermaphrodites (who invest less in muscle and brawn) from having sex. In some sense this is a variant of the first possibility: the comparative advantage of muscle is just so strong that the best solution is to have a division of labour. But it focuses not on problems posed by the environment, but rather on problems posed by one’s own species. If true, it feels a bit sad: that there could be a much better solution if it weren’t for the threat of physical force. But it does seem pretty plausible to me - especially because hermaphroditism is much more common in plants, which can’t use the strategy of physical dominance.

  • The main argument against it is that males in some species don’t compete via shows of force - e.g. birds which sing to attract mates. But birds are unusual in other ways too - e.g. over 90% of bird species are monogamous (as compared with less than 5% of mammals), which makes it more plausible that the "strong division of labour" hypothesis explains their sexual differentiation.  So I'd be interested in pointers to any literature on how many non-monogamous species lack physical male competition.
  • Also, in some species several different mating strategies remain in equilibrium (including strategies which involve surreptitious mating unnoticed by a dominant male). So even if physical dominance is the best strategy, is it really so much better that it can crowd out all the others?

Getting more clarity on this topic isn’t a priority for me, but I do think of the question as one small data point that might help ground big-picture abstractions about competition and cooperation (in a comparable way to how knowledge of how insect colonies works provides an interesting metaphor for thinking about society).

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My take is that it boils down to increasing the probability of fertilization, primarily in our early eukaryotic ancestors, in which sexual reproduction first evolved.

On the level of gametes (the reproductive cells), it's about the difference between isogamy (gametes being the same) and anisogamy (involving a larger and a smaller gamete, which are then by definition are the female egg cell and male sperm cell). The egg cells provide almost everything the eventual zygote needs to develop, while the main role of the sperm cell is to transport a set of genes to an egg cell. As it turns out, the sperm cell can do this with much less volume, and therefore, it is more cost-effective to produce them as small as possible, but in much higher numbers compared to egg cells. Making them smaller also makes them more mobile. Both high numbers and mobility help increase the chance of fertilization, especially in species with external fertilization, as the first animals would have been. When the fertilization is done externally, the animals don't exactly "bear" offspring, so there is no tradeoff in that regard.

Once there was a distinction between the gametes, other adaptations would have made sense, such as specialised organs for the deployment of eggs/sperm and traits that allow potential mates to recognize each other. The same goes for increasingly complex behaviour to ensure that those eggs and sperm are deposited in the right place at the right time and that the offspring develops well (including courtship displays, competition, nesting, brooding, etc.), much of which is sex-specific. Of course, in some animals this ultimately led to internal fertilization, where the benefits of anisogamy are not so relevant anymore, but the animals in question would have relied on a variety of sex-specific adaptations to even get to that point, and evolution only marches forward. The existence of some species that are hermaphroditic now certainly proves that it is possible to evolve in that direction, but as you say, there are surely various hurdles with fixating such a state on a large scale.

Yeah, this is pretty much the explanation I'm familiar with.

  • Gametes evolve, and two members of a species have to combine their gametes to reproduce
  • But having the same gamete that is both capable of moving out of the body and has the machinery for developing the embryo is inefficient.
  • So a division of labor evolves, where one gamete evolves to be easy to transfer (which causes it to be very small, which allows the production of much more of it), and one gamete evolves to receive the other gamete and have all the machinery required to create an embryo.
  • All other sex differences are then ultimately driven by this split - one sex has many small and cheap gametes they need to pass around to the other sex, and one sex has few big gametes that need to receive the other sex's gamete.

As for why not hermaphrodites that have both type of gametes, I think it's just inefficient, especially when you need many complex systems to support each one of the gametes. My understanding with hermaphrodite species like snails is that what drives it is their difficulty in finding a mate (because they're so slow), so when they finally meet a mate, it's best if they can just reproduce, and not have to go look for another.

Interesting! I don't think this answers the question of "why not hermaphrodites" though. A hermaphrodite can produce two different types of gametes, large and small (I assume this is what trees do). 

Yes, but the distinction between gametes had to evolve first from asexual, i.e., undifferentiated reproduction, while hermaphroditism requires some added complexities, as it has to combine both sexes in a way that works. And as long as divided sexes work well enough, there isn't much selection pressure to go that route.

As for why this is more common in plants, I'm intuitively guessing that there are a bunch of issues involved that I'm not familiar with either. But a major driver is probably that (land) plants are sessile and tend to require some space for themselves. The problem for plants with differentiated sexes is then that if their nearest neighbours happen to be of the same sex, the chance of their spores reaching those of the opposite sex is drastically lower than for hermaphodites, as the latter have potential partners in every neighbour.

This wouldn't generally be an issue in mobile animals, who have to find and approach their mates anyway.

This wouldn't generally be an issue in mobile animals, who have to find and approach their mates anyway.

Unless they're slow and uncommon as snails, in which case the cost of looking for a new mate might be high enough that developing hermaphroditeness was worth it. 

C. elegans, one of the simplest known animals, has hermaphrodites and males, with hermaphrodites massively outnumbering the males.

Perhaps being male is a strategy to make others bear your offspring, while you don't have to, and after a certain proportion of males in the population emerges, you might as well be female instead of hermaphroditic?

C. elegans, one of the simplest known animals, has hermaphrodites and males, with hermaphrodites massively outnumbering the males.

That's really interesting!

Perhaps being male is a strategy to make others bear your offspring, while you don't have to

The underlying question is: why would this strategy pay off more than also having your own kids? E.g. imagine a hermaphrodite equilibrium in which everyone wants to be impregnated by whoever has already borne the healthiest kids. In that equilibrium, males wouldn't have a chance - so why is the "some males" equilibrium selected instead of that one?

in which everyone wants to be impregnated by whoever has already borne the healthiest kids.

This would only possibly work in a species who kept track of these things. Aside from homanids, and maybe dolphins or elephants, most species aren't tracking who is who's child.

Also, being male means less resources on birth, so more on chasing a partner.

Nick Lane's book Power, Sex, Suicide has an interesting model for this that seems pretty different from any of the ideas here. It has to do with maintaining alignment between the eukaryote genome and the mitochondrial genome, and having just one mitochondrial genome makes that problem tractable. So sexual reproduction needs a way to only inherit mitochondria from one gamete, to which sex is the solution.

At the organism level, I think sexual differentiation evolves to specialize in the interests of the different gametes. For plants, it's straightforward to implement the different specialized strategies in parallel, but for animals its much more costly (they would have to carry around parallel adapted organs, and split time executing different behaviors).

I don't think the parallel adapted organs would be that expensive. Perhaps if you needed the secondary sexual characteristics of both sexes - but as I argued, in the long term we should expect selection for secondary sexual characteristics (and mating strategies) that were more compatible with hermaphrodism.

Evolution sucks at long term though - that's essentially your 4: they would be outselected before they would be frequent enough.

However, the "hermaphroditism is only found widely where, for one reason or another, finding a partner and finding them to be wrong sex can be really fatal" (sessile plants, slow snails) suggests it must be very costly indeed, and I'd bet on "simple" metabolic explanation: these adapted organs directly compete in terms of their influence on the body.

For cats, the female cat emits a mating call and multiple male toms typically hear the call and show up.  Then the toms have some kind of physical battle for dominance - with a lot of screeching you can hear - with the strongest, most aggressive tom obviously more likely to win.  The pair of cats do their business and the tom runs off, at which point the female starts round 2 of the mate competition...

This to me seems to be a stress test for robustness.  The tom has to perceive the female, navigate through non-home territory to her location, and survive a battle.  And to succeed he has to be able to do it on many nights, not just one, if he dies from wounds from the first battle his genes likely die with him.

This means the cat genes are constantly being stressed above natural environment stresses, for half the genes each iteration.  And yeah, for this to work the species has to afford failures, only a small percentage of the toms need to successfully reproduce each iteration.  Hermaphrodites don't have this 'disposable test animal' for evolution to check functionality each round.  

One thing that does not yet seem to have been mentioned is that it's unfavourable evolutionarily to have anything other than a 50/50 mix of males/females, as if there is a preponderance of one gender then if you are the opposite gender you'll tend to have more babies. Of course there are exceptions to this due to things like infanticide but on the whole it's a good approximation.

This does not explain how the first male came about of course, but it does explain how it only had to evolve once by chance and then immediately took over from there.

There are cases where artificially skewed gender balance can get corrected in a few generations:

https://www.theatlantic.com/science/archive/2016/08/the-strange-case-of-the-butterfly-and-the-male-killer/496637/

I don't have a total answer but I can make some predictions/contribute to the model:

 

  1. The more dimorphism between sexes in a species or niche, the less we should expect to see (simultaneous) hermaphrodism, because success as either sex requires costly investment. I think you're making a mistake dismissing this because physical dominance as rare- sex via physical dominance qua physical dominance is rare, it is much more often serving as a costly signal of resource abundance, which is exactly what bird songs are doing.
  2. Males are only deadweight loss if a population is producing fewer offspring than the environment can support. For a species at carrying capacity, twice as many offspring means twice the death rate. Therefor we'd expect to see hermaphrodism in k-strategists (which we don't, I'd guess because being a k-strategist already requires a number of costly investments) and in r-strategists that are frequently nearly wiped out locally, or finding new locations (I think this is true on the margin, although not overwhelmingly).

sex via physical dominance qua physical dominance is rare, it is much more often serving as a costly signal of resource abundance

This makes sense in pair-bonded species where the resources of the males help the females. But it seems like there are plenty of species where the male contributes very little, and so in those species the question is: why is the equilibrium of signalling resource abundance favoured over the equilibrium of signalling hermaphroditic fertility?

For a species at carrying capacity, twice as many offspring means twice the death rate.

Yes, but for any individual, twice as many offspring means that your genes make up a greater proportion of the next generation. So I think that this doesn't change the pressure towards hermaphrodism on an individual level (although maybe it makes group selection for it weaker).

I think we're in the uncanny valley where you're asking questions the literature genuinely doesn't address well, but also missing some stuff it has already covered, in ways that make it hard to work out through LW comments. This is an area of interest of mine and I'd love to discuss in person at some point.

Makes sense, let's chat directly!

I'm surprised that the major role of sexual selection seems to be overlooked. Sexual species can speed up evolution by magnitudes of order, because the selection can happen culturally, "in the minds" (only a metaphor!). In theory, any adaptive change can happen in a single generation at once, provided that the selective behaviour is able to change unanimously. Hermaphrodites wouldn't work that well, because there is no clear distinction between the group that you are competing with and the group you are competing for, which would probably make any behavioral strategy unstable.

Isn't sexual differentiation older and more widespread than sexual selection?

Hermaphrodites wouldn't work that well, because there is no clear distinction between the group that you are competing with and the group you are competing for, which would probably make any behavioral strategy unstable.

Why can't hermaphrodites just compete on a single axis, with the winners of that competition being the ones who get to impregnate others?

(Perhaps the benefits of winning that competition are so large that some will specialise in winning rather than child-bearing, and thereby become males. But not if the competitive criteria are strongly correlated with hermaphrodism - e.g. the single axis being "how healthy your existing offspring are" or similar.)

But in your scenario the offspring has only one "successful" parent. The best outcome for hermaphrodites would be for the "winners" to mate with each other, but then it might be unstable to switch between mating and competing behaviour between the same two creatures.

Hmm, I guess I don't really see why that'd be unstable?

Because it is probably hard to isolate the applications for each behaviour from each other. "Compete with A and mate with B as much as you can" is much easier to encode than "Compete with everyone, but then maybe at some point switch to mating with however you are fighting (but be careful that they don't take advantage of it)". You get the prisoner's dilemma at the very minimum.

PS If you think about it, even in humans, who do have sexual differentiation and are capable of very complex behaviour, those behaviours are not perfectly isolated, and external aggressiveness often leaks into the family. For me it is almost out of the question that such careful delineation could exist among primitive hermaphrodites.

Then why does it work well for plants?

What does? On the surface it seems that plants don't have sexual selection as they don't seem to be able to affect the choice of their "partner", so they don't have the advantage of proper sexual species. But maybe I don't know enough about plants.

I just spotted this paper, which is a little confusing but seems to be arguing that sex can be easily worthwhile when individuals can switch what sex they are in response to their environment. That seems basically equivalent to hermaphroditism, so in some sense it's just a restatement of the question I posed above, with more math.

It's not. It's really-really not. Having a switching ovo-testis is, while not cheap, far cheaper than a set of parallel organs which commit literally contradictory effects on your body simultaneously. Like, if we take humans, gestagen is used for chemical castration for a reason.

Huh. I like you spelling out the puzzle. I had the seed of a partial answer but hadn't noticed how incomplete it was before.

My guess had been that male expendability was a major evolutionary advantage. The fact that males can still have offspring after dying (because they already impregnated a female) means the evolutionary costs of deadly risk-taking drop by quite a bit. It also removes a lot of politics when it comes time to decide who has to risk death to protect the community from some threat. (If everyone's a hermaphrodite, it becomes a status thing. But if you have males, you obviously bias heavily toward risking losing males. Hence "Women and children first!")

I hadn't thought about it before, but it does seem to explain the animal/plant difference. This risk-taking thing isn't an advantage for plants. But it's super important for things that move and explore.

But I don't know how this would have first arisen.

I'm remembering some tickle of a claim that supposedly the human Y chromosome is a mutated X. That being male is a mutation and the default is female. I don't actually know what that would mean since human females would also have to have mutated (since they can't impregnate each other). But if there's a sensible interpretation, that strikes me as probably relevant to this question.

I think the X and Y chromosomes are a bit of a red herring. It's true that the Y is a degraded X, but in birds, males are ZZ and females are ZW. In both cases, the Y and W chromosomes slowly degrade due to their lack of a partner to do sexual recombination with. Eventually, the Y (and W) chromosome is (by default at least) expected to eventually disappear, but this does not mean males would disappear, instead the XY sex-determination system would evolve to replace the Y (and maybe the X too) with something else.

Right! 

IIRC this was also be related/causes to the fact that men suffer more genetic diseases (hemophilia? red-green colorblindness?)

Sounds like this is a combination of #1 and #5, depending on whether the risks come from the environment or from other males. But I don't think that "removing the politics" can be a general answer - maybe it's relevant for humans, but there are plenty of species which don't live in groups, or don't sacrifice very much for their groups.

My guess had been that male expendability was a major evolutionary advantage. The fact that males can still have offspring after dying (because they already impregnated a female) means the evolutionary costs of deadly risk-taking drop by quite a bit. It also removes a lot of politics when it comes time to decide who has to risk death to protect the community from some threat. (If everyone's a hermaphrodite, it becomes a status thing. But if you have males, you obviously bias heavily toward risking losing males. Hence "Women and children first!")

 

This explanation seems tailored to a particular ecological niche occupied by humans and very few other animals. It's interesting and I expect does have some effect on the margin, but for it to work as a general explanation for the existence of sexes:

  1. there have to be interventions where males can save their offspring in particular, not be generically helpful. This requires either a fair amount of physical isolation, or tracking which kids out of many are theirs and only intervening when predators attack those kids in particular, or having an ongoing relationship with the mother that almost certainly implies more paternal care. You can't have group level protection without strict gatekeeping, or males will freeride off of other males' protective efforts. I think e.g. chimps could theoretically pull this off via general social intelligence, and elephant seals because they're a harem species with a lot of physical isolation, but the conditions are not so common as to be an explanation for the general phenomenon of sexual specialization. 
  2. They also can't provide so much parental care that their death renders their offspring nonviable. In birds males can be equal parents post-egg-laying, but species typically do so only when offspring demand so much care a female cannot do it themselves. There are intermediate versions of this- maybe paternal death leads to half their offspring dying from lack of food, but not all. 

This exact question is discussed in Matt Ridleys The Red Queen. He puts forward that it's better for evolution in more unpredictable environments where variation becomes an advantage and vice versa for stable environments. It's a great book I'd recommend it.

The main thesis of the book is that because every other member of the species is evolving through generations you have to evolve at some rate even to stay still relative to other beings

To clarify: the wiki article mentions sexual selection but not the existence of sexes. Richard's question is "why don't we have sexual selection without sexes". Does the book talk about that?

There's a chapter on the evolution of sexes in Nick Lane's The Vital Question ("Sex and the origin of death"). It explores the benefits and costs of sex.
If I recall the big benefit of sex is gene shuffling (allows for recombinations, ie. faster experiments). Also it apparently evolved very early (didn't need much new machinery, benefits significant).