Sexual selection, which is a subset of natural selection, is defined as “selection based on mate choice.” It usually, but not always, takes the form of males competing for access to females, and results in the development of either armaments in males that help them compete in the battle for mates (antlers on deer, horns on stag beetles, etc.), or bright plumage, coloration, adornments, calls, or behaviors of males that catch the fancy of females (the bowers of bowerbirds, the plumage, colors, and strange behaviors of the New Guinea birds of paradise, the songs of male frogs, etc.). We understand the competition scenario more than the “female preference” scenario, for it’s hard to figure out why females would prefer one plumage or adornment rather than another.
Nevertheless, the signs of sexual selection of living species are fairly clear (males have the weapons or adornments, females don’t), and we can do tests to see whether sexual selection seems to be a reasonable explanation. In peacocks, for example, you find that males (the ones with the big tails!), who have more “eyespots” in their tails get more mates, sage grouse who display the most vigorously also win the mate race, as do African widowbirds with longer tails.
It’s harder to do these studies in extinct species, but a new paper by Knell et al. in Trends in Ecology & Evolution (reference below), gives some nice examples of possible sexual selection in fossils, as well as a list of things about the fossils that might indicate sexual selection.
First, a few fossils suggestive of sexual selection:
Of course, features like the fan-shaped crest above could have had other functions (e.g., thermoregulation, species recognition, etc.), so we have to use other criteria, delineated below, to see if sexual selection is a likely explanation.
Here’s a weird one—perhaps the strangest trilobite of all, Walliserops trifurcatus from the Devonian of Morocco (Photo: Dr. B.D.E. Chatterton). Check out those horns and the bizarre trident on its head. Richard Fortey showed this one at a talk I saw in Madrid last year, and I believe he gave a functional explanation for it rather than imputing it to sexual selection. (The photo, by the way, is of a real fossil.)
Now, how can we get an idea whether such bizarre features arose by sexual selection as opposed to other mechanisms (direct natural selection not based on mate choice, genetic drift, as nonadaptive pleiotropic byproducts of other features that evolved, and so on)? The authors suggest five observations:
- Sexual dimorphism. This is the most obvious feature: if an exaggerated trait or ornament is found in only one sex but not the other (preferably males), that suggests sexual selection. There are a couple of problems here. First, if you see two forms of fossils, one with a trait and one without, those could be males and females of one species, or they could be two different species, one of which has ornaments in both males and females. Also, there are forms of mutual sexual selection, in which males and females both prefer a trait, that could lead to both sexes having ornaments, and thus no difference to be seen in the fossil record.
But here’s one lovely example from the paper in which sexual selection is likely. It occurs in pterosaurs, flying reptiles of the Jurassic. As the TREE article notes:
Darwinopterus is a small pterosaur from the Middle Jurassic of China, known from numerous specimens. Some individuals are crestless, whereas others possess a bony crest located along the midline of the skull, which was probably associated with soft tissues that enlarged crest size substantially in life [77]. Crested specimens have a proportionally smaller pelvis and ventrally fused pelvic elements, whereas crestless specimens have an unfused, wider pelvis. Furthermore, one crestless specimen has a pterosaurian egg preserved in close association with its pelvis and so is clearly a female.
Here’s the uncrested female Darwinopterus showing her egg (arrow) immediately outside the cloaca (photo by Lü Junchang):
And here’s a reconstruction by Mark Witton that shows the sexual dimorphism of Darwinopterus:
- Change in growth rate during development. Because sexually selected traits are “expensive” in terms of metabolic/reproductive cost, and could make animals susceptible to predation, in living animals they tend to show up only at the end of development, when the animal is an adult and ready to reproduce. Indeed, that’s exactly where we’d expect to see them develop given the modern theory of evolution. And this is indeed the case, as is seen in things like peacock feathers and deer antlers. If one sees this in one sex of fossils (as we do with the bony crests of pterosaurs), it suggests sexual selection.
- “Positive allometry”. This means that as the body of an animals gets bigger during growth, the feature gets proportionally bigger than that. For example, if the linear dimension of body parts increases by a factor of 2 during development, sexual selection might be indicated if the size of the ornament increases by a factor of 3.5. This is really related to the previous point; neither are conclusive, of course, because one can have such positive allometry for other reasons, for example simply because of the constraints of development or biomechanical reasons. To deal with this, the authors suggest testing whether the degree of allometry is one expected under a hypothesis of sexual selection versus hypotheses like thermoregulation or use as a rudder (as in the crests of flying dinosaurs).
- “Morphological disparity”. This means that if there are related species in a group in which one or more species show evidence of sexual selection, that group will show a diversity of different traits that are elaborated. For example, the birds of paradise of New Guinea are sexually selected, with the males having bright ornaments, coloration, feathers, and bizarre courtship behaviors, and yet the traits of males differ drastically among related species. This is probably because female preferences vary erratically among different species (I won’t go into why this might be the case), and so the males also come to differ. Click on this Google image search that shows some of the “morphological disparity” among sexually selected males in those birds.
- Costliness. Sexually selected traits tend to be “costly”: that is, they take a lot of metabolic energy that could be diverted to other traits, or even reduce survival by making the male bearer visible to predators. Male peacocks are not only highly visible to predators because of their coloration, but their long tails make it hard for them to fly. Of course, if such traits are sexually selected, the advantage gained by attracting more females has to outweigh the “cost” of bearing the ornament; and experiments in some species show that this is indeed the case. As the paper explains, if traits arose for another function, say to recognize members of the same species, one wouldn’t expect them to be so costly.
Remember that these features are indications of sexual selection in the fossil record, not absolute proof (which we don’t get in science anyway), and it’s hard to test various alternative hypotheses. The evidence for sexual selection becomes stronger if the traits in a fossil species show a combination of the different properties shown above. I find the example of Darwinopterus (above) pretty convincing.
I’ll leave you with one more example of a fossil species that might have experienced sexual selection: this is a Cambrian trilobite, Parablackweldeeria luensis (from the paper), showing a fossil (a) and reconstruction (b). The animal was unusual in having its eyes on the ends of long eyestalks:
This resembles the long eyestalks shown in diopsid flies, like this speciemen of Teleopsis dalmanni, in which males have eyes on long eyestalks as a result of sexual selection (the males “face off” against each other and butt each other with their heads; long eyestalks give an indication of head size and may help settle contests by forcing the smaller fly to give up sooner.
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Knell, R. I., D. Naish, J. J. Tomkins, and D. W. F. Hone. 2012. Sexual selection in prehistorical animals: detection and implications. Trends Ecol. Evol. Early online publication, Sept 7. DOI 10.1016/j.tree.2012.07.015
Now this IS one sexy post!! Yeah science. My brain sure loves this kinda stuff.
Darren Naish (one of the authors) has a post at Tetrapod Zoology at scientific american blogs see here
http://blogs.scientificamerican.com/tetrapod-zoology/2012/09/07/sexual-selection-in-the-fossil-record/#respond
Dave Hone (err, me) one of the other authors of this paper also has a post on this at his (err, my) blog here: http://archosaurmusings.wordpress.com/2012/09/05/sexual-selection-in-the-fossil-record/
Reading this site is always a great education. Thanks for this analysis.
>>We understand the competition scenario more than the “female preference” scenario, for it’s hard to figure out why females would prefer one plumage or adornment rather than another.
What do you mean by “why”? If you mean “how it comes about” then I thought that is already a well understood phenomenon. There’s no particular evolutionary benefit for one plumage over another but once by chance a particular plumage becomes slightly more fashionable than others, then it becomes a disadvantage for ones sons not to have that plumage. And so the plumage soon becomes dominant.
If you mean “why” as in “what is the purpose” then it the answer is that the question is invalid. The birds would not really be thinking about purposes at all, anymore than we are thinking purposes when selecting “sexy” mates, and we have more capable brains.
That’s the part that’s poorly understood. Is it really just arbitrary whim (‘by chance’), or are there reasons why preferences evolve (which may then get washed out by further runaway selectionas you have described)? Many female preferences seem not arbitrary at all, but serve as more-or-less honest indicators of male genetic quality.
I think arbitrary, just like fashion in human culture. You see it happening faster in culture. There’s no “reason” for thin ties versus wide ties, or short shorts versus baggy, etc. We could think up “reasons” after the fashion catches on but that’s more rationalizing after the fact. And *we* can rationalize but not birds.
In human fashion the constant changing is one of the salient features. The necessity of keeping up with it shows that you have both the money to be constantly replacing your clothes (when they almost never wear out) and the time to pay sufficient attention to know what the fashion is. Both of these are costly and indicate genuine genetic fitness, at least in some areas.
The curious thing about that analysis is that it attributes reasons for the behavior, that people almost never think about when they buy fashion items. People don’t think it’s going to show they have money. They actually think that the in-fashion items look good, and the out-of-fashion is distasteful.
There is of course such a thing as conspicuous consumption, but nobody conspicuously consumes out-of-fashion things.
…or the fashion is different so that we have a speciation event?
It’s hard to imagine different fashions arising within one population. Even in culture, there has to be some separation in cultural millieu. For example there could not be a single population of birds half preferring red-feathered males and the other half preferring blue-feathered males. I don’t see different “fashions” occuring unless there is already population separation.
The preferences must start very weak and subtle. And the accentuation of the adornment both in the display in the carrier and the strength of the preference in the chooser grows over time. It won’t be like one day a mutant bird gets born with bright red plumage and another with bright blue, and the females have to choose between them.
Female preference really isn’t that mysterious. R. A. Fisher settled that one back in 1930 or so.
The reason for the initial preference of the female isn’t important. It may signal fitness, differentiate between similar species, or just be a random side-effect of genes selected for some other reason.
Once the female desires more X, where X is the trait in question (size, length, color, spots, etc.), you end up with a runaway chain reaction that increases that trait to the breaking point. That’s because the offspring produced will have genes for both creating and desiring the trait in question.
At the end of that process (which is typically when the male can no longer survive with a “better” version of the trait), the significance of the original root preference is completely obliterated. If a slightly longer tail once indicated better survivability somehow, the monstrosity on a widow bird certainly does nothing of the sort today (quite the contrary). So fitness, in the colloquial sense, can be diminished while fitness in the Darwinian sense increases.
Actually, two previous commenters, the issue of female preference, which is thought to precede the evolution of male traits, actually is quite mysterious. There are in fact at least seven or eight hypotheses about why females might prefer one trait rather than another, including direct benefits, the good genes model, the runaway theory (random preference), antagonistic coevolution, preexisting bias, and so on. I suggest consulting a book like Futuyma’s Evolution before you say that the issue is “settled”! There are many suggested reasons, and probably all apply in some instances. Figuring out which is the one responsible in a given case is, as I say in the book Speciation (cowritten with Allen Orr), very, very hard.
what Jerry sez.
Ok. I misunderstood the original post. I read it as a problem of choice from random traits.
In cases of direct benefit, or indicator traits, or pre-existing bias, I think of these as cases where there’s really no female “choice”. Her choice is forced because there is some real penalty for not choosing the right plumage.
In the case of the runaway random preference, this is what I considered more as a “preference” issue, where the choice is not rigged from the start. I guess the “one plumage rather than another” phrase threw me off. 🙂
You’re using the word mysterious differently than I do. If I have a grasp of some pretty basic physics, and see a few thousand balls come bouncing and rolling toward me, I don’t consider their behavior mysterious simply because I don’t know where each one began rolling or falling.
As I said, the initial reason for the female preference can be anything. My whole point was, it does not matter, since that does not figure into the mechanism of sexual selection. It’s like asking why proto-whales like Pakicetus ended up living near the shore, when the real story is what happened after they did.
“..the issue of female preference … actually is quite mysterious.”
Well I could have told you that when I was 15!
So what you are saying is that for millions of years the males of many species are just trying to figure out what a girl wants?(he,he)
Two comments. Jerry’s definition of sexual selection leaves out one of Darwin’s two mechanisms—male-male competition. In some cases, mate choice may work in concert with male male competition but sexual selection can occur only due to male male competition without females showing any preference whatsoever. Second, in response to a reader, Fisher’s runaway is not the only explanation for the evolution of female choice. Direct benefits like food or a good territory, indirect benefits (good genes in offspring) and sensory aspects are also possible explanations. Also note that while Fisher provided a possible explanation, there is still no direct evidence that supports only Fisher’s mechanism but no other mechanisms. Doesn’t mean it does not occur; it is just extremely difficult to show.
My definition was simply selection based on mate choice. That includes male-male competition because only males who win the contests get to even choose a mate. And, as Allen and I point out in my book, it’s not clear that females don’t CHOOSE to mate with the guy who wins a contest. A deer who wins, for example, doesn’t automatically get to have a given female: she may have to choose whether to mate with that winner or not. This may be the case with leks, for example, and this issue is an unexamined aspect of male-male competition.
eh. I didn’t like the definition either. Some sort of ‘choice’ ,may or not be happening in purely intrasexual (male-male combat) scenarios, but not necessarily.
Better to say that sexual selection is ‘differential reproduction due to differetial mating success’ as opposed to other components of fitness like survivorship, fecundity and the indirect benefits of kin selection.
I’m not sure I like your definition any better. Does a salmon’s ability to climb waterfalls count as “differential mating success”?
Seems to me (as an interested non-professional) that the clearest cases of sexual selection are those that involve a choice of mating partners.
(sub)
Salmon, male or female, that don’t get to the spawning grounds have zero reproductive success. That’s much more like survivorship–everybody has to live long enough for even a shot a reproduction. The competition for mating success per se occurs once they’re there.
It’s not “my” definition, by the way, but Darwin’s, and it’s the one in use by people who study the topic, like Andersson and Arnold (to name just 2).
Fair enough, if that’s the definition that’s actually in use. But it still seems somewhat arbitrary to say that getting past a predator or a geographic obstacle is survivorship, whereas getting past a rival male is sexual selection. They’re all part of the environment that must be overcome in order to mate.
There are always the males who do not win but still mate with the females – it happens with Cervus elephas. Didn’t Maynard Smith call them ‘sneaky fuckers’? The females are not coerced – there is perhaps an advantage in having some gamete competition rather than male v. male competition.
Thanks Jerry. Your posts on evolutionary theory are always a highlight for me. 🙂
Agreed!
If we look at it from a “survival circuits” brain perspective:
– The male items are predominately displays, noises or extra/larger body appendage, fighting
– These require more energy output by the body of the male.
– They likely also demand more energy consumption and acquisition
So they seem to signal extra energy that is available to and thru specific males. As mentioned, male male competitions let the males expend energy to do the initial filtering of energy resources and capabilities.
It seems, then, that sexual selection may be a darn efficient way of finding, in the immediate ecosystem — today — excess energy resources that can be co=opted for offspring. Conception being almost instant, it is the shortest of time frames and must get the calculation of “best” right — right now.
So then are females selected to be more discriminating? Have sharper perception of cues? That should be testable.
This is so cool! Definitely going into my lectures! Thanks Jerry.
Great post! Tnx
JAC quote:-
Electric field detector as per sharks? In his marvellous 2011 lecture at the 150th anniversary of Oxford University YOUTUBE VIDEO Fortey says ““I have no idea what the trident was for”
It looks like it waves through the top layers of the sandy/muddy sea-floor looking for small buried animals to eat, to me.
yes. That’s what I meant, but didn’t write.
Unless I’m sorely mistraken, human female breasts fit all five categories, which would mean that it’s not just male competing for females but also the reverse.
This one needs no explanation.
Change in growth rate during development. Because sexually selected traits are “expensive” in terms of metabolic/reproductive cost, and could make animals susceptible to predation, in living animals they tend to show up only at the end of development, when the animal is an adult and ready to reproduce.
Menarche and thelarche are generally simultaneous in humans, or at least not separated by very many years.
“Positive allometry”. This means that as the body of an animals gets bigger during growth, the feature gets proportionally bigger than that.
See thelarche, again.
“Morphological disparity”. This means that if there are related species in a group in which one or more species show evidence of sexual selection, that group will show a diversity of different traits that are elaborated.
The female breasts of other great apes are nothing like those of humans. Other great apes have other “showy” features, such as the hood around a male orangutan’s head.
Costliness. Sexually selected traits tend to be “costly”: that is, they take a lot of metabolic energy that could be diverted to other traits, or even reduce survival by making the male bearer visible to predators.
I’ve known more than one woman who had breast reduction surgery to alleviate chronic back pain. One poor girl had them grow back even bigger after the surgery….
So…any comments from the real evolutionary biologists out there?
Cheers,
b&
Apologies for some formatting failures, especially the lack of indentation of the quoted bits….
b&
it’s a puzzle.
link
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You can just imagine the conversations, say, between a student researcher and the parent: “I’m paying how much so you can stare at pictures of breasts all day long?”
Still, going by the five criteria Jerry listed, it would seem unlikely that sexual selection isn’t a significant factor.
b&
Considering that trilobites were bottom dwellers walking along the sea-floor looking for things to eat, I’d be more inclined to think these eye-stalks were about a better field of view myself. A fly which can err, fly is less in need of stalks to see better.
See this trlobite Erbenochile erbeni which had even more fabulous eyes which I think, look like they are about better vision in order to find prey.
http://www.trilobites.info/Erbenochile.jpg
There were pelagic trilobites as well. Jerry posted a Richard Fortey video a while back that went into some detail about such critters.
I do agree, though, that sexual selection would not be the first thing that comes to mind when I see those eye stalks. I think of lurking in the seabed waiting for prey.
Great post Jerry, I think I’ve learned more about evolution and biology from you and PZ in the last couple of years than I learned before. I find myself wishing I had become a scientist when I was younger.
Cheers!
I couldn’t take the sad kitty face, Professor Coyne, so I’ll offer a caption for the illustration of Darwinopterus by Mark Witton:
“Where have you been all night? Crawling in here at 3AM… and you NEVER wear your crest like that! Who is she?!?
I also appreciated this quote:
“This is probably because female preferences vary erratically among different species (I won’t go into why this might be the case), and so the males also come to differ.”
I won’t go into why. 😉
The Darwinopterus crack wins the thread!
I’d like to thank the A-Cat-emy, and especially Ceiling Cat, for this award…
@Marella: we used that example specifically to make the point that some of the time with fossil material it’s really hard to use analogy with extant organisms to understand function. You can draw an analogy with Diopsid eyestalks and conclude that trilobite eyestalks were probably sexually selected, or you can draw an analogy with some extant crustaceans that have their eyes on short stalks and conclude that they were probably adaptations for seeing over soft sediment. Alternatively, they could have functioned in both ways (and we need to remember that while diopsid eyestalks are primarily sexually selected they also give some visual benefits as well). If you drop me an email I can send you a copy of the paper where we discuss this in a bit more detail.
ps Nice write-up Jerry, thanks.
Rob Knell
I will give my two cents worth on the subject of religion but even I can realize there are subjects that I am not even vaguely qualified enough to give an opinion.I still find this post informative and fascinating though. Please continue posting subjects on biology.
Jerry, why do you write “preferably males” in your discussion of sexual dimorphism? As an ornithologist, a contrary example immediately came to my mind. All of our North American species of phalaropes are polyandrous. Females are distinctly larger than males (as much as 43% so), are more colorfully plumaged, and compete with each other for territories, which translates as access to males. A female with a resource-rich territory might have as many as four males each incubating a clutch of her eggs, and she provides no parental care to the young. Admittedly polyandrous species are less than 1% of all avian species. But the phalaropes famously fooled John James Audubon, who mislabeled the sexes in his paintings of these species. Since he at least field dressed the birds before mounting them to paint, he clearly was a way better painter than he was a biologist.
Probably no way to know, but I’d argue there could have been polyandrous species in previous eons, since they’re out there today.
Preferably but not inevitably. I had in mind the exceptions (including also seahorses) when I wrote this. I talk about seahorses and, I believe, phalaropes, in WEIT as exceptions to the male-ornamented rule.
We understand the competition scenario more than the “female preference” scenario, for it’s hard to figure out why females would prefer one plumage or adornment rather than another.
Our animal ancestors were Neil Strauss fans, and eventually his Peacock Theory was embedded in the genome as it occurred alongside various other advantageous, if not somewhat toolish, techniques. “Wow, nice tail plumage. Is it fake?” “Ha, totally got in a great neg!”
Great post. Look at me, learning things in the hopes that the sad kitty picture will be replaced. I didn’t realize evolution could be so… I don’t know, inefficient, in a way? I thought it was all about functionality, interesting to find out otherwise!
so, basically, what you’re saying is, that there is no evolutionary advantage to liking candy corn, and that it does not represent runaway sexual selection among diabetically-inclined hominins?
So after millions of years the guys still haven’t figured out what a girl wants? (he,he)
nice try!!!
http://www.creationartnsoul.com/id40.html
Help me here. If I understand this correctly a preference for traits that would sexual select for mates that have lower reproductive success would result in having this behavior eventually disappearing from a population. Would this not mean that sexual selection does not compete with regular selection but rather simply magnifies its effect. Big flashy displays may be costly but they are displays that I am a fit mate who is able to make lots of fit offspring.
Reblogged this on Mark Solock Blog.
Very interesting article and I’m happy to see sexual selection gaining new interest. A question for you, Jerry, re your taxonomy of theories: why is sexual selection “a subset of natural selection”? Darwin considered it a parallel force and in fact proposed it as separate theory because it works very differently than natural selection. In fact, it often works at cross purposes to natural selection – for example, with the peacock’s tail – so how can a force that works at cross purposes to natural selection be considered a subset of natural selection?