THE BLOG
03/04/2013 06:07 pm ET

Was Darwin Wrong About Sexual Selection?

''... the manner in which the individuals of either sex or of both sexes are affected through sexual selection cannot fail to be complex in the highest degree" (Darwin 1859 p 296).

Everybody seems to know that sexual selection is the process that results in fancy traits in males because females are choosy and males profligate and competitive. Putting aside that these sex-difference "truisms" are not always "just-so" and that they sometimes fail to capture even the "average natures" of males and females, sexual selection hypotheses are part of Darwin's legacy that I and other Darwinians like me celebrated last month.

You already know the usual sexual selection chorus: Female choice and male-male behavioral competition sort among males so that the biggest and strongest males are the winners of the mating game and the smaller, weaker, and common-place males are the losers, leaving females as choosy and gloomy (hmm... not unlike the loser males), so that a universal expectation is that guys are horny and bellicose (hmm... except when they're not) and gals are coquettish and judicious (hmm... except when they're not).

But beyond these trivialities (and mysteries), modern day confusion even among professionals seems fairly common. Consider what happened at the International Society of Behavioral Ecology meeting in Perth, Australia where there was a breakout discussion called, "What is Sexual Selection?" Participants said they wished to discuss, "how to define sexual selection." Oops! It seems even professionals forget Darwin's essentials and get muddled. Of course, there was the brouhaha that Joan Roughgarden's book and later papers stirred when she claimed, "Sexual selection is wrong" Then a National Geographic cover blared "Was Darwin Wrong?" To add to the sense that somehow we are all adrift in a sea of controversy, there is a forthcoming book from contributors to a 2011 Paris conference, "What's Left of Sexual Selection?"

I am happy that I am a contributor to the book-to-be as I greatly admire Darwin's selection hypotheses and think what I have to say might surprise some readers familiar with my skeptical attitude to some investigations of sexual selection.

To be clear: No, I do not think all fancy male traits arise via sexual selection. Nor, do I think that sexual selection only happens among males. No, I do not think that the only ways sexual selection happens are through female preferences and male-male competition. No, I do not think there is a "direction of sexual selection", because sexual selection can operate simultaneously on males and females and be simultaneously extreme or not in both sexes. Yes, I think some modern Darwinian acolytes cast crude caricatures of Darwin's great hypotheses. Nevertheless, Darwin's selection hypotheses are testable, hypothetico-deductive statements, rules if you will, of the form "if this and this and this are true, then this new thing is so." That is not wrong, that is brilliant.

Thinking about the assumptions of Darwin's hypotheses lifts the miasma of confusion over "how to define" sexual selection. If this and this and this are so, this other thing must also be so. That's it. Read Michael Ghiselin's important book if you need more explanation, or consult Dan Dennett who said, selection is like arithmetic.

So what are these first principles, the "this and this and this" above? One assumption is about the units of selection -- who carries heritable variation and lives and replicates or fails to replicate and dies. Check out Richard Lewontin's classic paper if you are still confused about units of selection.

A second assumption is one about the mechanisms of selection (how does the environment vary and affect the units of selection). No one's been better than Darwin (maybe Wallace) on how the environment might "wedge" or sort among the units of selection. Darwin is readily available and open-access, online and free. You should take a look!

A third assumption is about the component(s) of fitness that thereby vary among the units of selection. Darwin went on and on about survival and reproductive success.

If one is stating a hypothesis of evolution via selection, there is a necessary fourth assumption about the details of "information transfer" between generations (i.e., about heredity via genes, culture, learning, epigenetics of gene-environment interactions). The advanced class includes Fisher's The Genetical Theory of Natural Selection and as well as books and papers of the other architects of the neosynthesis, and continues with Maynard Smith and Szathmary's Major Transitions in Evolution and Mary Jane West-Eberhard's Developmental Plasticity and Evolution.

Darwin said that sexual selection is a kind of natural selection, because as you remember he was contrasting his idea of natural selection to artificial selection in which farmers and herders picked who would breed and who not. In contrast to farmers' picking this one to breed because it was fat, pretty, or bizarre, Darwin's natural selection just happens. There is no instigator. There is no target of selection. Natural selection happens whenever there exists heritable (genes, culture, their interaction via epigenetics) variation within a population among individuals (the unit of selection) because the environment varies, so that some individuals because of their traits fail to thrive, breed, or survive in that environment. Natural selection is a very broad hypothesis.

Sexual selection was among the first of Darwin's "narrow sense" natural selection (i.e., not artificial selection) hypotheses. Each of the assumptions of sexual selection was more precise, "narrower" -- and more readily testable because of greater precision -- than the assumptions of the broadest natural selection hypothesis. Narrow-sense hypotheses proliferated, and the wars of naming conventions began. If the units of selection are individuals of a single sex within a given population, selection is among individuals within a sex. Thus, some called all hypotheses focused on individuals within a sex "sexual selection". Other moderns took female choice and male-male competition to be the defining metric, and they declare as sexual selection only those formulations having to do with female choice and male-male competition as sexual selection. Other moderns enamored with the so-called "wicked" selective efficacy of variation in number of mates, limit "sexual selection" to those selection hypotheses assuming effects only through variation in number of mates.

In other words, fights over naming conventions are less substantive (think of fog and Cheshire Cats) than the head scratching suggests.

If Darwin were around, I suspect he would ask his acolytes to stop yelling and to enumerate their assumptions. You know: if this is so and this and this and this, then this new thing, evolution via selection, must also be so.

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