In humans, males tend on average to be larger, to mature later, and to age and die sooner than females. It’s easy to assume, as many people do, that this difference between males and females — what biologists call sexual dimorphism — is the result of sexual selection. That is, males are larger because they fight each other over access to females and/or females prefer to mate with larger males. That is a valid hypothesis, of course — but too often it is simply accepted as fact and then used as a starting point for discussing other male and female traits. As a recent example, consider the debate that is happening on the blogosphere about sexual dimorphism in humans, and whether objections to the standard explanation of fightin’ males is merely political.
It started with PZ Myers’s post “Keep your biological reductionism off us men, too“, to which Jerry Coyne responded with “The ideological opposition to biological truth“. In response to Coyne, Holly Dunsworth provided a critique via blog and Twitter, the latter of which is summarized here. UPDATE: Coyne responds here and here.
I will avoid the political aspect of this discussion and focus on the science involved in the debate, because I think it highlights an important issue: namely, the need for evolutionary biologists to consider and test alternative hypotheses, even if they are not as intuitively plausible as the main hypothesis. This is one of the reasons that evolutionary biologists often take issue with claims from evolutionary psychology — because evo psych often tends to present a plausible hypothesis but does little to critically evaluate its underlying assumptions and even less to present and rule out alternatives. In particular, evolutionary biologists should know better than to restrict the list of hypotheses ones based on selection, because there are usually viable non-adaptive hypotheses as well. Natural selection is not the only mechanism of evolution.
So then, how should an evolutionary biologist approach the example of sexual dimorphism in humans? What alternative hypotheses could there be to the standard explanation? Well, here are some comments that I once wrote up for a student who made the typical “males are bigger/mature more slowly/die sooner because they fight over females” assumption.
Three male characters are listed: 1) larger size, 2) slower development, 3) faster senescence. One hypothesis, direct intrasexual selection (i.e., male-male combat), lumps them all together and explains all three with natural (sexual) selection acting on that trait. That is one possibility. It is also four testable hypotheses rolled into one (i.e., that the three traits evolved under selection related to mating success, plus that they are all part of the same adaptation).
Alternative view #1 is that these are adaptations but they’re decoupled and evolved separately. For example, maybe large size evolved due to sexual selection for male-male combat, but slower development evolved to provide time to learn about hunting. Alternative view #2 is that they evolved together but one or more is a byproduct of another. For example, slow development is simply necessary in order to reach larger size with larger muscle mass and is not in itself adaptive (i.e., if it were possible to become large quickly, this would evolve – indeed, there are good theoretical reasons to expect fast time to first reproduction to be strongly favoured, all else being equal). Alternative #3 is that they are decoupled and not all of them are adaptations. The point is that although these traits are all consistent with the hypothesis of male-male combat, it is not a given that they are coupled in their evolutionary history nor that all three are the product of selection.
Next, we would need to consider as many plausible explanations as possible for each of the three traits.
1) Larger size in males:
Adaptive hypotheses type 1: Males selected to become larger
– Male-male combat (direct intrasexual selection)
– Mate guarding (indirect intrasexual selection) and/or dominating reproductively active females (inter-sexual conflict)
– Female choice (intersexual selection), either direct (good genes if a male can manage to become large) or indirect (large males can provision offspring with food – maybe demonstrated by providing food and other items to females, which would certainly be consistent with modern human behaviour)
– Males hunt large/strong/fast prey and females don’t, so males need to be larger/stronger/faster (ecological selection)
– Males but not females go to war frequently with other tribes over access to food and other resources (group selection or kin selection, as you like)
Adaptive hypotheses type 2: Females selected to become smaller
– Smaller body size means reduced requirements for food, more can be invested in offspring
– Smaller body size can be achieved more quickly during development, allowing reproduction to get underway sooner
– Smaller body size may have been preferred by males as a secondary sexual characteristic
– Smaller body size may be a byproduct of other changes in developmental timing in females
2) Slower development in males:
Adaptive hypotheses type 1: Males selected to develop slowly
– Adaptive because it provides time to develop the size and skills needed to face competition with other males
– Adaptive because it provides time to develop the size and skills needed to hunt large prey
– Adaptive because it provides time to develop the size and skills needed to fight rival tribes
Adaptive hypotheses type 2: Females selected to develop more quickly
– Faster development is adaptive because it means earlier age at first reproduction (leading to higher potential lifetime reproductive output)
– Getting larger simply takes longer / being smaller takes less time (if growth rates are similar in males and females)
One might argue that the non-adaptive explanation is the simplest, so we would need evidence for why we should reject it and add a more complex explanation in its place Then you would need to test the primary adaptive hypothesis and the alternative adaptive explanations.
3) Faster senescence in males:
– Adaptive, in the sense that male mortality due to combat is high so there is investment in early reproduction rather than anti-senescence, whereas the opposite occurs for females
– Adaptive, in that males consume an inordinate amount of food such that earlier death of males favoured under inclusive fitness
– Adaptive, in that males are selected to reproduce as much as possible while young regardless of whether most offspring survive whereas females are selected to invest in a few offspring over the long term and to see them through to adulthood (r- vs. K-selection)
– Non-adaptive – males have higher metabolic rates than females, which means more oxidative damage
– Non-adaptive – testosterone, which contributes to large size, aggression, and sperm production, has the long-term effect of hastening senescence but this is not selected against because it increases reproductive success earlier in life (antagonistic pleiotropy)
Again, I think the non-adaptive explanation is the simplest and indeed there is evidence that testosterone has this effect (castrated males live longer, for example). So again, there would need to be evidence against this as well as evidence for a particular adaptive explanation as well as evidence against alternative adaptive explanations.
Add onto all of this the question as to why sexual dimorphism is not more pronounced in humans than it is, especially if it is thought to have evolved after we became non-arboreal. Are there developmental or genetic limitations (constraints)? Or stabilizing selection acting on another trait?
Finally, there may have been a reduction in overall sexual dimorphism during hominin evolution from Australopithecus to Homo. This would mean that stronger sexual selection (and/or other) pressures existed long before modern humans evolved. Fossil data are limited on this, but it’s clearly a relevant issue.