Friday’s New York Times contained an article on sexual selection in birds (link and title in the picture below) by Richard O. Prum, the William Robertson Coe Professor of Ornithology, Ecology and Evolutionary Biology at Yale’s Peabody Museum of Natural History. Prum has a new book out, The Evolution of Beauty: How Darwin’s Forgotten Theory of Mate Choice Shapes the Animal World — and Us, which I intend to read. For now, though, he’s given us a take in the Times which is both erroneous and confusing, for it misrepresents sexual selection, natural selection, and modern evolutionary theory.
Here’s the Amazon summary of the book, which explains how Prum is trying to revive Darwin’s theory of sexual selection—a theory, which, by the way, has not been forgotten, but either refined with additional assumptions or discarded outright because Darwin didn’t know genetics or had no evidence to support his views:
In the great halls of science, dogma holds that Darwin’s theory of natural selection explains every branch on the tree of life: which species thrive, which wither away to extinction, and what features each evolves. But can adaptation by natural selection really account for everything we see in nature?
Yale University ornithologist Richard Prum—reviving Darwin’s own views—thinks not. Deep in tropical jungles around the world are birds with a dizzying array of appearances and mating displays: Club-winged Manakins who sing with their wings, Great Argus Pheasants who dazzle prospective mates with a four-foot-wide cone of feathers covered in golden 3D spheres, Red-capped Manakins who moonwalk. In thirty years of fieldwork, Prum has seen numerous display traits that seem disconnected from, if not outright contrary to, selection for individual survival [JAC: We’ve known this for a long time: it’s reproduction, not survival, that is impelling the evolution of these male traits.] To explain this, he dusts off Darwin’s long-neglected theory of sexual selection in which the act of choosing a mate for purely aesthetic reasons—for the mere pleasure of it—is an independent engine of evolutionary change.
It’s true that Darwin was the first person to ponder sexual dimorphism—the extraordinary difference in ornamentation, weapons, and behaviors between the sexes—and to speculate about its causes. He suggested “sexual selection”, and gave two hypotheses about how it worked.
The first, which Darwin called “the law of battle,” was correct: males are larger and have weapons or features that enable them to compete for females, as when elephant seals or elk fight it out for mates. The ultimate cause of this difference, which I’ve described before, is the difference in gamete size between the sexes (sperm vs eggs), which ultimately leads to females being a scarce resource for which males have to compete. I won’t describe it further; you can consult a good evolution textbook, such as Futuyma and Kirkpatrick (it shows some examples of sexually selected traits on the cover below), or read the Wikipedia article on sexual selection, which is okay but not great. Lots of experiments and observations confirm that males do fight over females, and the weapons and their size make a difference. (Males also compete for females after fertilization: the so called “gamete competition.” One example is in damselflies, in which a male, before inseminating a female, will use a scoop on his penis to remove the sperm of the previous male. The selective advantages of having such a device are obvious.)
Darwin’s second theory, however, was largely wrong, as it was based on females preferring certain traits of males because of their appeal to the females’ aesthetic sense. Here are the two theories given by Darwin in his 1871 book, The descent of man and selection in relation to sex.
“The sexual struggle is of two kinds: in the one it is between the individuals of the same sex, generally the males, in order to drive away or kill their rivals, the females remaining passive; while in the other, the struggle is likewise between the individuals of the same sex, in order to excite or charm those of the opposite sex, generally the females, which no longer remain passive, but select the more agreeable partners.”
The problem here is that it takes the aesthetic sense of females as a given rather than something that can itself be the product of evolution. And of course it implies abilities not present in many species, like flies, who surely don’t have “aesthetic senses”. While Darwin’s “aesthetic” theory can be modified to take into account pre-existing female preferences that are either evolved or the byproduct of some other evolved trait (Ronald Fisher was responsible for this advance), in itself it doesn’t explain much. Darwin was correct, though, that female preferences can cause males to evolve traits that hurt the males’ survival (as in the elaborate tails of peacocks), so long as the males’ loss in “fitness” due to survival costs is more than compensated by their gain in fitness due to females mating more often with males having exaggerated calls, behaviors, or ornaments.
The mechanisms of sexual selection and causes for female preference still remain mysteries, for there are many reasons why females can prefer the traits of males that make them so bizarre—traits like the plumes, ornaments, and behaviors of the New Guinea birds of paradise. And distinguishing among these hypotheses—which include the “runaway hypothesis”, direct benefits models, handicap models, sensory bias models (a refinement of Darwin’s ideas), “good genes” models, and so on—is difficult, especially because they can work in tandem. To see the hypotheses for the evolution of female preference (which Darwin took as a given) and the difficulty of testing them, have a look at this 2009 PNAS paper by Jones and Ratterman. The paper shows this table listing the varieties of ways that female preferences for male traits can evolve:
In his New York Times piece, Prum ignores most of these, claiming that sexual selection is not a form of natural selection, does not lead to adaptation, and leads to “maladaptive decadence.”
Here’s an example. After describing the elaborate display of the male club-winged manakin, which lures females by rubbing together its wing feathers (a trait that has caused the evolution of thick, flight-impeding wing bones, and whose results can be seen in the video at bottom), Prum says this:
This [manakin song] is an evolutionary innovation — a whole new way to sing. But the evolutionary mechanism behind this novelty is not adaptation by natural selection, in which only those who survive pass on their genes, allowing the species to become better adapted to its environment over time. Rather, it is sexual selection by mate choice, in which individuals pass on their genes only if they’re chosen as mates.
It’s hard to make THREE errors in two short sentences, especially when the writer is an evolutionary biologist writing about evolution, but that’s what Prum has done. Here are the errors:
1.) Sexual selection is a subset of natural selection: the consistent differential reproduction of genes based on their advantage in replication. Sexual and natural selection are not two distinct processes. Here’s Futuyma’s definitions from the 3rd edition of his textbook.
“Natural selection” is defined as “The differential survival and/or reproduction of classes of entities that differ in one or more characteristics.”
“Sexual selection” is defined as “differential reproduction as a result of variation in the ability to obtain mates.” These definitions, which are held by nearly all evolutionists, clearly show that sexual selection is a subset of natural selection, the subset affecting traits involved in mate competition. Prum’s claim that the two processes are distinct is confusing and wrong.
2.) Prum conceives of natural selection as only differential survival, whereas it’s differential reproduction that is key. Differences in survival produce selection only if they’re associated with differential reproduction. (They often are.)
3.) Neither natural nor sexual selection necessarily leads to an improvement in “species becoming better adapted to their environments over time”. Selection most often operates on genes that affect the reproductive output of their carriers, but that needn’t improve the adaptation of a species to its environment. For example, a mutation that increases the number of a bird’s offspring, but has no other effect, will simply increase the number of young birds in the population, which isn’t an improvement in adapting to the environment. In fact, this could ultimately lead to a depletion of food that could drive a population extinct. Likewise, the mechanism of “meiotic drive”, in which one mutant gene simply kills the other genetic variants during gamete formation, is a form of natural selection that can and probably has driven populations extinct. Throughout the article, Prum seems to conflate adaptation (a phenomenon of genes and individuals) with the survival of a species or its adaptation to the exigent environment. While this can happen, it’s not a necessary connection.
Those sentences would surely mislead a reader who wasn’t acquainted with evolutionary biology.
I could go on, but I’ll give just one more example of misleading prose in Prum’s short piece:
Of course, females do not harm their own survival by choosing males with attractive songs; the costs are deferred to their sons and daughters. Although their daughters will inherit more awkward wing bones, their sons will inherit sexually attractive songs, resulting in more grandchildren.
In the absence of direct costs to the choosers, the population will not be saved by natural selection. Because the cost is deferred, the whole population can ease further and further into maladaptive dysfunction, generation by generation.
Evolved decadence may turn out to be common.
. . . The wing songs of the club-winged manakin teach us that adaptation by natural selection does not control everything that happens in evolution. Some of the evolutionary consequences of sexual desire may not be adaptive. Rather, they can be truly decadent. Despite the ubiquity of natural selection, organisms are not always getting better at surviving. Natural selection is not the only source of design in nature.
This is deeply misleading, and not just by confusing reproductive “fitness” with survival alone. Deferring the “cost” of choosing a clumsy-flying male by one generation doesn’t throw the population into a death spiral. In that next generation, if the cost of female choice outweighs the benefits of choosing those males, females will evolve in the reverse direction, choosing males that can fly better. There is no inherent force in sexual selection that will lead both males and females to evolve beyond their fitness optima. And if natural selection (including sexual selection) isn’t the only source of design in nature, what is? How does “decadence” produce design?
I hope Prum’s book is better than this excerpt. I showed his NYT piece to another evolutionist, who allowed that it was profoundly confusing. But the average reader, not deeply acquainted with sexual selection theory, will think that Prum has hit on some new principle of evolution. And in that way his article does the reader a disservice, for what he says is a mixture of stuff that evolutionary biologists already know, confusing and misleading characterizations of selection, and a neglect of competing and unresolved explanations for female choice—explanations that haven’t all been examined in manakins.
As lagniappe, here’s a club-winged manakin singing with its wings:
Is it that evolutionary biology (my field too) is more prone to these false or misleading claims of “novelty”?
I doubt it. I can think of many researchers in my field – psychology – who have built a successful career by rebranding something we’ve been researching for decades.
Surely “the difference in gamete size between the sexes (sperm vs eggs)” is not a cause of sexual dimorphism, but one example of it. The ‘ultimate cause’ is that symmetrical sexual strategies are not evolutionarily stable… ?
Yes, true; I was taking gamete size dimorphism, which can evolve on its own, as the starting point.
A quick Google search for books on sexual selection undermine the claim that the theory has been forgotten or neglected. An EBSCO search (or Google Scholar, for that matter) for journal articles destroys it.
Matt Ridley wrote a popular book on sexual selection called The Red Queen. This guy must have been living under a rock.
I’d like another cup of kerosene, please…
It’s an astonishingly ignorant claim: look at any recent edition of the major behavioural ecology journals and there will be multiple sexual selection papers – it is still one of the most active research areas in behavioural and evolutionary ecology
To be clear: “It’s an astonishingly ignorant claim” by Prum
“And of course it implies abilities not present in many species, like flies, who surely don’t have “aesthetic senses”.”
Exactly how do you test this statement? I ask in all seriousness since I’m continually amazed at some of the clever experiments scientists use to test things.
I would think any sort of “not-obviously functional-aspect-of-a-conspecific-detector” could be regarded as something along the lines of aesthetic sense.
(Characterizing beauty and other aesthetic categories is a difficult enterprise in my view – though I did try once for computational reasons.)
Why should being functional disqualify a sense from being aesthetic? If a fly gets pleasure from anything at all, surely it gets it from the sight or scent of a potential mate. That’s how natural selection motivates adaptive behavior: by making it feel good.
Likewise that plant that flowers once a year – and smells like something dead – attracting numerous flies to pollinate it. We would find it disgusting but the flies find the smell beautiful because it smells like food and a place to lay their eggs. I was thinking also re Prum’s comment
“Of course, females do not harm their own survival by choosing males with attractive songs; the costs are deferred to their sons and daughters. Although their daughters will inherit more awkward wing bones, their sons will inherit sexually attractive songs, resulting in more grandchildren.”
Well actually such females do affect their survival by deciding to reproduce – because of the heavy investment in food and energy – in raising their young – whereby they no doubt may risk their lives just as the male with extravagant plumage or battling competitors does. Consequently it is in her interest for the object of attraction to also have features that give a good chance of those young – in whom she is so invested – surviving. Hence it makes sense if the attractive characteristic also confers or is offset by some characteristic that makes the young likely to survive to reproduction. Moreover the young can be seen as an extension of both herself and the male through their combined genes – which explains the investment of both sexes. This fits the natural selection that is genetic oriented explanation as in WEIT, Fisher et al, as opposed to the purely natural selection explanation
I was concerned that would make “aesthetic” worthless by making it apply to everything. I do admit that I was acting somewhat “behaviouristically” – you added the “pleasure” bit, which perhaps can help. Don’t know.
Well no: motivated behavior doesn’t always correspond to what feels good. Wanting and liking are separable, though overlapping neural systems. Kent Berridge has a lot of relevant studies. Useful summary here.
The author of the article is same as all those evolutionary biologists who claim that the neo-Darwinian synthesis is wrong,sacred dogma, and they’re being the good guys and trying to lead it into he right path. Because people, readers, love to hear about these kind of stuff. I don’t know why he claims that sexual selection is neglected topic, isn’t the work of Amotz Zahavi – handicap principle all about sexual selection? I don’t know your opinion about Zahavis work but I certainly know the the topic of sexual selection is not neglected or forgotten and I’m not an evolutionary biologist.
I have always liked Zahavi’s handicap principal, and signaling theory more generally, but I am not an evolutionary biologist either.
Principle
Well, it could have been worse. At least he didn’t write about group selection. I do remember being very confused as I read that and wondering why an evolutionary biologist was writing about natural selection and sexual selection as two distinct processes. I was a bit distracted reading it and didn’t fully process it, so thanks for pointing out some of the errors here. This is helpful.
Two tangentially related questions for Ceiling Cat:
(1) How come nobody ever mentions Charles Darwin’s grandfather, Erasmus, and how he influenced/shaped his grandson’s work? Do you think he should get more credit and/or be mentioned more often?
(2) Why are some evolutionary scientists so keen on challenging Darwinian evolution today? We know some of that challenge comes from a place of ideology (specifically when it comes to sexual dimorphism), but, at least in this case, that doesn’t seem to be true — at least from the small amount of information I have at hand here in this blog post. So from where does this particular challenge discussed in this post? Is it sheer ignorance, a wish to make a name for oneself, or something else entirely?
It’s common in all branches of science, people determined to out-darwin darwin, out-einstein einstein, etc it’s based on the premise that nobody no matter how brilliant can think of everything so there are always a few crumbs for others to fight over.
Oh, I certainly am aware of that trend, but it seems some particular theories of Darwin’s are singled out. I mean, when it comes to someone like Einstein, people were right, and I think even Einstein knew he was only beginnning/on the brink of something, not the be-all and end-all theorist on the subject.
But they don’t just want to outdo them, they have a compulsion to show they are “wrong.”
I have seen the manakin (decadence) argument in the past used as a reason for why the dinosaurs became extinct. Apparently they put so much effort into growing in size, dcreating crests etc to attract mates that the line declined into exhausted extinction.
Perhaps the manakins should take note.
How ironic that manakins are dinosaurs.
😆
Isn’t that one of the strengths of scientific enquiry?
Cheers,
Haggis
Must say I never understood why sexual selection was/is considered as a different mechanism from natural selection rather than a ‘special case’ of natural selection. (But then, Wallace didn’t want to have any of it, so it is nothing new).
I think , and Prum is a clear example, that natural selection is seen as ‘survival of the fittest'(a phrase by Spencer, not Darwin) instead of the ‘reproduction of the fit enough’ (don’t remember whose that one was).
I think that Darwin left the causes of female preference wide open. I think he would have been very interested in the different causes proposed now. But that is, inevitably, speculative.
Isn’t Prum merely trying to distinguish (albeit awkwardly) between a Fisherian/Lande process, where female choice is initially for an arbitrary male trait that doesn’t benefit females directly or indirectly, and all other direct or indirect benefit (good genes) models?
I do think that most animal behavior types dismiss Fisherian/Lande processes for no good reason, and so in that respect Prum has a valid point.
Sexual selection must explain not only sexual dimorphism, but also the rapid divergence of male secondary sexual traits between closely related species. All of those benefit models fail to do that (what would be the adaptive reason to change female preference if its already adaptive??), whereas Fisherian/Lande easily explains why such rapid divergence is likely.
In this article Prum also seems to be of the opinion that selected traits, via Natural Selection, have to increase fitness. That just isn’t the case, not per modern evolutionary theory anyway. At least that is only true with respect to other traits experiencing selection pressures at the same time, but not with respect to an organism’s evolutionary history. In other words species can become less fit than they were in the past due to traits acquired by Natural Selection. Or at least that has long been my understanding, but I am not a biologist.
Although I agree with you regarding Prum’s forgotten sexual selection and several other points, I beg to disagree with the definitions of natural and sexual selection defended here. Charles Darwin, who coined and defined both terms, considered them to be separate concepts. Natural selection was selection by nature “guided” by ecological factors that led to ecological adaptation: things the natural theologians he fought would call ‘useful design’. In contrast, sexual selection was, for Darwin, selection that resulted from social factors affecting mating success, such as males fighting among themselves for mating opportunities or female choice that favored some male phenotypes over others. Features evolved through sexual selection not only do not promote ecological adaptation, they will usually be hostile to it: in this I agree with Prum. As evidence against Paley’s natural theology of universal utility, sexual selection demanded a pedestal of its own.
The separation between the two forms of selection is useful on historical grounds, respecting Darwin’s usage and insights (Darwin already had sexual selection pinned down in the 1840s), and, more importantly, because ecological geneticists and behavioral ecologists find it useful separate the two because of their different natural history ramifications and subsequent research traditions. I myself, however, would never criticize someone who preferred, because of his or her scientific or philosophical viewpoint, to consider sexual selection a subset of natural selection, even though it confounds a distinction many biologists find useful.
It is true that once selection, whether natural or sexual, is underway, the underlying genetics and molecular biology are the same; however, this provides no solace to mere naturalists with other fish to fry. Many lab geneticists probably wish sexual selection, with all its intricacies, would go away. The issue of definition is not new, and some (myself included) have indeed chosen to call Darwin’s natural selection “individual selection” to avoid such semantic scuffling.
I also disagree with the third point, that a mutation that increased offspring number would not be an adaptation because there is no benefit to increased competition for food, etc. However, the individual(s) carrying the trait would be “fitter,” in leaving offspring in the environment. An adaptation, in Darwin’s view (IMHO), was a ‘winning strategy’ in the war with nature (ecology). Darwin walked the fence on this. He would claim that ecological adaptations produced by natural selection would tend to increase population size but at the same time seemed to recognized that Malthusian factors could negate the advantage, but not the selection. [As for meiotic drive, sex distorters and the like, they are just natural selection and adaptation acting on levels below
organismic advantage: No Problema].
As for your second point, I suspect that Prum, in writing “natural selection, in which only those who survive pass on their genes,” merely committed a small gaff (and that he knows better) of the kind embodied in Spencer’s dictum “survival of the fittest”, which people who know what it means still use despite its blatant inaccuracy.
Also, I don’t think Prum is trying to imply that sexual selection puts populations in, to use your expression, “a death spiral”. I do, however, think he is hyping his tale with the term “decadence”. But then again, we have the Irish Elk, don’t we, and didn’t its giant antlers make it ‘decadent’ to the point of extinction? (maybe by ending up as Neanderthal barbecues).
I have been fortunate enough to witness the red-capped manakin song and dance routine in nature; just amazing.
Why single out the ‘Irish Elk’? Was not most of the pleistocene megafauna eradicated? I do not think at all, and there is no evidence whatsoever, that it disappeared because of its large antlers. (A if I missed some sarcasm, plze forgive me, it was not clear).
The few cave paintings of the ‘Irish Elk’ (as popularised by the late S.J. Gould) show an animal where the bump on the shoulder was a more prominent feature than the antlers. And the latter were kept low, contrary to the image painted by some more recent ‘reconstructions’.
I agree they probably were an item on Neanderthal and/or Cro Magnon barbeques.
Some sarcasm, but not all. Big antlers (IMHO) were a drag on male elk and took them closer to their energy threshold or made them easier victims for primitive hunters. Like Jerry implies, I believe (still in IMHO mode)that natural selection ameliorates the negative adaptive effects of sexual selection to some kind of optimum and will not by itself lead to extinction — the “Too Sexy to Survive” bit. However, it might make a species susceptible to unexpected stress, like an Ice Age.
Some find that sexual traits resulting from Fisher’s brilliant runaway model, which I personally do not believe is important in nature,cannot be opposed by natural selection [it has been a long time since I last read up on this stuff]. I have often wondered if Fisher himself believed in his model or that he just made it up in a effort to provide some kind of logical explanation, in 1930, for how innate female preference might lead to male ornaments.
Taxonomists sometimes explained male ornaments by the need of females to have identifying marks to recognize the male of the species and avoid the costs of either hybridization or mating failure. This view appears to lack much factual support and (IMHO) seems sexist.
Sexist why? Is someone sexist to observe that a group of species may have easily identified males and seemingly uniformly drab females. That does occur in nature, you know. If it’s a problem with taxonomists [especially arthropod specialists], most are always tweezing out genital structures, and in many groups seeing baroque species-by-species variation in males, not so much in females. But these structures are rarely on display to females, and I doubt anyone believes these are “identifying marks” exactly.
In groups that have good vision and where there is visually obvious variation between species in males and not so much in females, it’s hard to think that female cost-analysis and female choosiness is probably operating.
I disagree with you on the definition point. I think that one can have sexual selection remain a useful term and still be a subset of natural selection. There is virtually no way to have sexual and (non-sexual) natural selection be completely distinct mechanisms and attempts to do so (various workshops have tried)get bogged down in semantic goo.
Jerry defends sexual selection as being a sub-set of natural selection, which also implies that SS is definable. Keeping SS as separate and distinct from NS — making traits of interest an either-or-both-neither proposition — is certainly useful for behavioral ecologists, but not so much so for evolutionary geneticists.
This does not make sense to me. I agree with Jerry’s point—sexual selection is a subset of natural selection. I thought you were disagreeing with this perspective and if so, sorry about the misinterpretation. Note, however, if sexual selection is a subset of natural selection then it cannot be distinct and separate.
I indeed disagree with the usefulness of combining SS with NS. Darwin defined them as distinct processes. Fields of modern science that specifically study SS treat it as separate from NS. By doing this statements made concerning the evolution of the natural history of plants and animals can be clearly stated without requiring distracting qualifications. Evolutionary and other biologists who do not work with SS seem to see the problem as exclusively a question of concept classification: NS and SS act on genes in the same fundamental way, only SS has the special feature of acting only through relative mating success. In this view, SS should be considered a subcategory of NS The stinger is that mating success involves a labyrinth of male-male, male-female,and female-female behavioral relations, evolutionary mating games, strategies, tactical deception, occult advantages, etc. that are different from, and rival in complexity, those that affect the NS of ecological adaptation. Reason requires that NS and SS be considered apart, at least by specialists.
I fundamentally disagree. The main difference is which aspect of fitness is affected– mating vs other. And, I actually do study sexual selection so I could as a biologist who works with sexual selection. There are contexts of classic natural selection (fitness not connected to mating) that give rise to the same sorts of traits as sexual selection). I will send Jerry a post on this soon.
should have written “I could count as a biologist who works with sexual selection”
You make a lot of good points! I think you can go even farther though…
You talk about adaptation to environment and adaptation to produce more offspring, but do not link the two and make the ultimate observation that the animals themselves are part of the environment, hence adaptation to produce more offspring is, in reality, just a form of adaptation to the environment.
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The topic here is sexual selection. I hope that no one assumes that the pigeon in the larger photo on the cover of the Futuyma and Kirkpatrick book is an example of it. The bird appears to be of a domestic breed of rock dove whose fancy feathers were artificially selected for.
No, I said that SOME pictures reflect sexual selection. Pigeons, which humans find nearly impossible to sex visually, are obviously not an example.
I find it disheartening that the NYT devotes its pages to such misinterpretations of evolution.
A minor correction: I think that the first “fertilization” in the post should be “insemination”.
Yes – too late to scoop out the semen if fertilization has already occurred!
Despite solid wing bones and specialized secondaries, the club winged manakin can’t be that ‘decadent’ because it’s listed as least concern. It must fly well enough to get food and avoid predators. So much so that it hardly seems like a death spiral of out of control maladaptive female preferences.
Yes, in order for a trait to spread individuals with the trait need to have more surviving offspring on average than individuals without the trait. This involves both surviving long enough to be able to reproduce and being attractive enough to win mates. Even in strikingly sexually dimorphic species with males that possess dramatic sexual ornamentation there must still be a compromise between ‘sexiness’ and ability to survive. At some point further increases in the size of the peacock’s tail will so handicap him that it places an upper limit on tale size even if females would show a preference for even larger tailed males if they were available.
It is pretty common for people to teach that sexual selection is different from natural selection, rather than being a special case of it. So it would be understandable that an educated person would simply repeat what they were taught. But this is supposedly an evolutionary biologist, so its surprising.
I can speculate that it is a case of careerism. Maybe he wants to make a name for himself well outside of academia.
Mark, I am also a (supposedly) evolutionary biologist who, like Prum, uses sexual selection and natural selection in the Darwinian sense (vs. the Fisher, Haldane, Wright tradition defended by WEIT) of conceptually distinct processes. Numerous workers and respected publications also have not hardened around this genetics-mandated use. Three examples follow in which my assertion seems to be supported by the article’s title:
M. M. Kasumovic and M. C. B. Andrade. 2006. Male development tracks rapidly shifting sexual selection vs. natural selection pressures. Current Biology, 16 (7): R242-R243.
C. R. Archer et al. 2015. Sex-specific effects of natural and sexual selection on the evolution of life span and ageing in Drosophila simulans. Functional Ecology, 29:4, 562-569.
Peter O. Dunn et al. 2015. Natural and sexual selection act on different axes of variation in avian plumage color. Science Advances, 1 (2), e1400155.
These titles would not make sense were sexual selection defined as a subcategory of natural selection.
Cheers!
Holy cow, that manakin song is incredible. I had no idea such birds existed.
And thanks for the write-up, Jerry!
Woodcocks also make a song with their feathers, but not sitting still. The sound is made as they perform aerial maneuvers. I have never seen what the actual flight looks like, because they begin the flight-dance just as it is getting too dark to see. Wonderful to hear, though.
Yes, the dive-zzzzt! or dive-vrrt! wing-notes occur in several birds. In much of North America, the nighthawk is a familiar example. Always associate it with warm summer nights along a row of apartments with suitable flat pebbled rooftops.
When it comes to sexual selection being a subset of natural selection, I’m curious as to sexual selection in animal classes. Mammals and birds and many fish engage in the subset of sexual selection. I can’t think of any reptiles that do. Does a penis scoop on a damsel fly equate as sexual selection?
I’m curious as to how sexual selection has evolved among classes. And is there a class that started it; earliest examples?
Thanks for this post. The best since you left for NZ imo. 🙂
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Charles Darwin defined natural and sexual selection to be disjoint concepts. In the 1930s population geneticists hijacked Darwin’s term and redefined natural selection to include sexual selection. Prum appears to be aware of this history, while Coyne does not. Yet Coyne sees fit to lecture Prum on the meaning of these terms. Pfft.
Well-known theoretical biologist Mary Jane West-Eberhard seems to take Prum’s side and defend (see “Darwin’s forgotten idea: The social essence of sexual selection.” 2014, Neuroscience and Biobehavioral Reviews 46: 501–508*) the separation of Sexual Selection and Natural Selection and the idea that SS has been neglected by the mainstream. West-Eberhard writes, “The Darwinian concept of sexual selection as social selection has been repeatedly forgotten within evolutionary biology, beginning soon after publication of Darwin’s treatise on the subject (for a concise history of reasons see Andersson, 1994). Sexual selection amnesia also characterizes many modern discussions of sexual selection, which often emphasize the importance of natural selection for the evolution of sexual signals and female choice. When that happens rich possibilities for insights regarding the evolution of male and female neurobiology, behavior, and morphology are inadvertently lost from view.” Although this text is 3 years old, it almost sounds like she wrote it to defend Prum. Since I have not read the entire article or searched the reference she cites, I cannot vouch for the validity of her assertions (which like Prum’s, seem a bit extreme).
*free pdf download
Readers will take my comment with caution as I have no scientific training but it seems to me that Prum’s comments are also cause for concern as they strongly imply or at least open the way for some version of intelligent design or else Gouldian social constructivism. Whether or not Darwin separated Natural selection from sexual selection or not he was not a geneticist and modern genetic knowledge undermines Prum’s assumptions. Even Fischer in the early 20thC noted heterozygote advantage – an diploid (sexually reproducing) organism with two different alleles (active differentiation bits) of a gene. Such diversity produces the well known phenomenon of “hybrid vigour”. The vast majority of Eukaryotic organisms reproduce sexually. Nick lane in Evolution Ascending explains reasons for the development of sexual reproduction as being a way to edit out both viruses and germs and most mutations (by using two sets of genes from separate organisms, then the cutting up and total gene recombination process of forming the embryonic cell. Large mutations are almost always harmful, but a collection of small mutations are more likely to be adaptive. And the ones that kill or maim the organism are not going to be transmitted. Hence sexual selection edits out big mutations and allows for development of stable species of increasing complexity. Thus the more complex asexually reproducing species e.g. dandelions tend to have a much shorter existence as species than sexually reproducing ones.
Please correct my errors where Im wrong but the geist seems to me that sexual selection is linked to natural selection in that the former balance out to service the latter as in hybrid vigour – the bigger a population the more variety of alleles and more incidence of heterozygotes and that many apparently purely aesthetic or attractive traits are linked either to traits that further successful rearing (territory, protection, parental assistance, fertility etc) or are indicative of health and stamina (e.g. long and elaborate songs). Thus sexual selection which place considerable stress on survivability in the environment will naturally tend to balance back to natural selection unless there is some sudden change in the environment.
And another thought (perhaps a bit mischievous) If the attraction of the female that is the target of sexual selection in some species were for example purely “aesthetic” then why aren’t female birds assiduously trying to attract the mating attention of other attractive species? And even a peacock only lives in dense tropical forest where it can fly enough to find a secure post and if it is healthy enough to grow such a large and splendid tail it must be quite strong.
Here’s a paper about a different bird that also evolved wing bone structure with auditory qualities — here seen as a reliable (index signal) warning indicator
Hingee, M. and R. D. Magrath (2009). “Flights of fear: a mechanical wing whistle sounds the alarm in a flocking bird.” Proceedings of the Royal Society of London B: Biological Sciences: rspb20091110.
My concern with Prum’s editorial was his insistence that the choice was “aesthetic”, with no signaling or other function. It seems more likely (and scientifically fruitful) to assume that there is some value in a behavior, but we don’t understand it (yet).
And “choice”, at least choice based on mental comparisons, cannot hold in the case of gamete competition, as when females’ reproductive system seem to recognize as use the sperm of one male over another’s.
Perhaps the closest i come to seeing Prum’s point is to think about why that particular “aesthetic sense” evolved. If they had evolved a preference for a particular sensory experience in some other realm, and it carried over as a by-product/overgeneralization in their mate choosing process, you would have the “decadent” spcies decline he describes. But it still would not be an “aesthetic sense” unmoored from any evolutionary process.
Andersson’s book Sexual Selection is over 20 years old, but is nevertheless chock full of still-debated hypotheses and data-rich examples:
http://press.princeton.edu/titles/5522.html
Prum is well aware of all the other models explaining the evolution of sexual ornaments by mate choice. As stated in the article, his main concern is that so little empirical attention is paid to the Fisher model especially in comparison with the good genes or fitness indicator model. I think he has a point there. His hunch (because good empirical data are currently lacking due to research bias) is that the Fisher process plays a much larger role than is assumed by the bulk of evolutionary biologists and psychologists. I am not sure about that, but he is right that we can’t know if we don’t take the Fisher process seriously.
What does seem problematic to me in the Atlantic article is that he pitches the subjective experience of beauty (which he links to the Fisher process) against good genes sexual selection. Yet, pleasure is a proximate mechanism, while good genes is an ultimate function. As such they are orthogonal and cannot be pitched against one and another. As if assessing sexual ornaments that reliably indicate quality cannot be pleasurable because they are utilitarian.