Why Evolution is True is a blog written by Jerry Coyne, centered on evolution and biology but also dealing with diverse topics like politics, culture, and cats.
Peacock spiders are not only beautiful, but great examples of sexual selection, for the males show both amazing colors and fascinating display behaviors that they use in their attempts to attract females. “Attempt”, of course, doesn’t mean they’re behaving with conscious intent, but just showing the results of sexual selection.
The only reason peacock spiders don’t get as much attention as, say, their avian counterparts—the birds of paradise—is that they’re tiny, like this (all photos by Jurgen Otto):
Like all salticids, peacock spiders are also lightning fast, as you’ll see in some of the videos below.
I’ve written about these arthropod jewels before (here and here); they are, as I said, salticids, or jumping spiders, and peacock spiders fall in the genus Maratus. All but one of the 50-odd species (there may be 60 or more) are found in Australia. Their primary popularizer and discover is Dr. Jürgen Otto, who has a video site devoted to them as well as a Facebook page and a Flickr page.
As is typical of sexually-selected species, only the males show bright colors and displays, which ultimately result from reproductively competent females being a scarce resource that must be attracted.The video below shows the amazing variety of behaviors of Maratus spiders (51 in this clip). Males frantically wave their legs and abdomens (all strikingly marked) to get a female’s attention.
Otto has a mildly disturbing habit of adding dance music to the spider videos; I prefer to turn the sound off. One can appreciate these creatures without anthropomorphizing them:
Here’s one species, Maratus volans, discovered, filmed, and narrated by Otto (at 5:21 you see an unsuccessful male eaten by a female):
Two years ago Otto described seven new species of Maratus; here’s a video showing those:
Now, according to several sources, including the Australian Broadcasting Corporation, Otto’s found four more species, as well as a new subspecies. Annoyingly, none of the articles reporting this discovery cite or link to the scientific paper with formal descriptions (this is a flaw in a lot of science journalism). I finally found Otto’s paper in an obscure journal, Peckhamia, with a citation and free link at the bottom of this post.
If you click on the screenshot just below, you’ll go to an ABC video that shows all of the new species:
And here are the new species. First, the abstract of Otto’s paper:
Four new species of the genus Maratus are described from Western Australia: M. cristatus, M. electricus, M.gemmifer, and M. trigonus. M. electricus is compared to the closely related M. linnaei Waldock 2008. A new subspecies of M. melindae Waldock 2013, M. melindae corus, is reported from a new locality east of Cervantes. The courtship display of all six species is also documented.
Go to the paper for a lot more photos, as well as pictures of the females, which are similar and much less colorful than the males shown below:
Maratus electricus:
Maratus cristatus:
Maratus gemmifer:
Maratus trigonus:
M. melindae corus (it has not escaped my notice that this species looks very similar to M. gemmifer pictured above, but it’s identified in Otto’s paper as a subspecies of a different species, differentiated by color markings).
Reader Charleen sent me the tweet below, which shows the courtship ritual of the hooded grebe (Podiceps gallardoi), a rare and critically endangered species (fewer than 1000 individuals) that lives in isolated Patagonian lakes. Have a look at this craziness, and ask yourself “Why the hell are they doing this?” or “What selective advantage is there in testing each other this way?” And don’t ask me, because I have no idea! It’s clearly a bonding ritual, but may be a form of mutual sexual selection in which potential mates size each other up in some way:
That in turn led me to a new article in Audubon magazine that identifies the clip as coming from a new movie about the species, “Tango in the Wind.” Fortunately, the half-hour documentary is free on Vimeo, and I’ve put it below. Grebe species are known for some really fancy footwork during courtship (Google “courtship grebe”), but the Hooded takes the cake. And, as Audubon notes,
But the Hooded Grebe’s courtship hasn’t been nearly as well documented [as that of other grebes], thanks to its limited range in the harsh and isolated barrens of Patagonia, near the tip of South America. In fact, the species wasn’t even known to science until 1974. “There aren’t many people who know much about Hooded Grebe courtship,” says Audubon field editor Kenn Kaufman. “The people who made this video probably know as much about the bird as anyone does.”
. . . The Hooded Grebe’s courtship dance may look funny, but with fewer than 500 breeding pairs remaining, this is serious business. Its numbers have declined by about 80 percent in the past 25 years, largely due to the introduction of the non-native American mink and rainbow trout, according to BirdLife International. The International Union for the Conservation of Nature labeled the species critically endangered in 2016.
Researchers interviewed in Tango in the Wind say climate change further threatens Hooded Grebe’s habitat and survival, noting that it’s already drying up the lakes where they nest. While more abundant than their Patagonian cousins, Western Grebes and Clark’s Grebes both face significant losses of their summer range, thanks to climate change. They’re among the 314 climate-endangered North American bird species identified by Audubon.
Now, if you have half an hour, watch this lovely but sad movie—sad because this wonderful species is on the verge of extinction, probably due to global warming. And watch it on full screen; the link for that is here. (The courtship segment begins about ten minutes in and you can see a bit at the very end.)
About 20 months ago we discussed the amazing Peruvian lyre-tailed nightjar, with its fabulous streamer feathers. This morning a rather different, and extraordinary nightjar tailfeather adaptation popped into my inbox, thanks to the Nightjar News email newsletter. It included information about the Standard-winged Nightjar (Caprimulgus longipennis), which sounds kind of… standard, until I realised that by ‘standard’ they mean ‘flag’. Here’s a picture of a male, by Paul Cools.
Those things behind him are his tailfeathers – they are what prompted the species name: longipennis (long feather). Nightjar News explains:
The Standard-winged Nightjar is one of the more impressive members of the Caprimulgid family. This true nightjar species breeds in dry savannah habitat of central Africa. During the breeding season, the male grows highly-specialized wing feathers up to 38 cm long, primarily of bare shaft with feather plumes on the end. The feathers are used as part of a flight display to attract female.
Here’s another picture, from Wikipedia, taken by Jan Steffen:
These long feathers look pretty sexy, and you can see why a gal might like them, but there’s more! Look at how extraordinary they are when he flies (there’s no sound, sadly) – video by Dermot Breen:
Sometimes, the display can look like the bird is followed by two bats:
Here’s another example, from the Gambia – at the end you can hear the male churring:
It seems fairly certain that this is an example of sexual selection – only the male has the feathers, and he has them only during the mating season.
However, this insight is only the beginning of wisdom, for it raises a whole set of questions:
• What exactly does the female see (or maybe hear)?
• Is it simply the length and shape of the feathers she likes, or is there something about the way he does the display that somehow reveals his ‘good genes’ (this is one of the key ideas about how sexual selection works, though in fact we generally know very little about what is ‘good’ about those genes)?
• What exactly is it about the display? Is it ‘supposed’ to look like two birds following him (why?), or is that just an aerodynamic consequence of having those long streamers?
• And here’s the real killer question – how on earth could we find the answers to these hypotheses?
Please chip in below…
[EDIT: On reflection, it seems like there is a difference in the behaviour we can see. In the first video, the male is flying very low, with the ‘standards’ upright, like flags. I wonder if this is a mating flight. In the second video, ‘three birds or one’, he’s flying like a hungry nightjar, with the feathers jiggling along behind him as he does his hunting flight, jinking around trying to catch insects. In the third video, he’s just mooching about and then starts his call… My guess is that the first behaviour is the key one, in terms of sexual selection.]
The Cornell Birds-of-Paradise Project is a great website that contains all kinds of information about the 39 species in this fantastic group. There are videos and information about the sexual dimorphism in plumage and behavior, and other aspects of the birds’ biology, information about their evolutionary history and the people who study them, and general information about evolution and sexual selection—even a video on speciation. It’s a remarkable and informative site: the best place to visit if you want to see what are the most stupendous examples of sexual selection—and I’m referring not just to the male behavior, but to the female choice that drives much of it. It’s a rich resource for those who teach evolution.
Below is a 4½-minute video of the famous Superb Bird of Paradise (Lophorina superba), whose Cornell page is here. I like this video because it’s not just a “gee whiz–look at this!” presentation (you can see Attenborough’s shorter video of this species on a previous post), but one that shows how at least four different groups of feathers have evolved, and conspire, to create the “smiley face” appearance of the displaying male. There are also several evolved changes in male behavior, including jumping around to stay in front of the female and raising his bill to bisect the blue crown feathers.
After an evolutionist has gotten over her amazement, the first question that then arises is, “Why is the male bird doing this?” That is, what, exactly, is the female looking for that makes her not only drive the evolution of this display, but makes some patterns and behaviors more acceptable than others? Good genes? Some pre-existing sensory bias in the female?
In fact we know almost nothing about what drives this genre of “female choice” sexual selection. This means that, for the time being, we can only marvel at it, and at the power of natural selection—of which sexual selection is a subset.
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.)
This book isn’t cheap, but if you can have only one evolution textbook, this is the one to get.
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:
Just when you think you’ve seen everything amazing that animals can do to attract a mate, you find something even more bizarre. This short video from BBC Earth shows a male pufferfish off Japan working tirelessly to build a stunning “sand castle” to attract females. Narrated by David Attenborough (of course), this video blew me away.
As National Geographic reports, the circles are two meters wide, take ten days to build, and, if one pleases a female, she lays her egg in the nest, and then the male fertilizes them and guards them till they hatch six days later. Then the male builds a new nest all over again. The discovery was made by Hiroshi Kawase et al. and published in 2013 in Nature Scientific Reports (reference and free link below).
A beautiful nest:
A male pufferfish (center) made this nest to lure females in Japan in 2012. Photograph courtesy Kimiaki Ito
Patricia Brennan is an evolutionary morphologist who teaches at Mt. Holyoke College (her website is here), and her speciality is animal genitalia. As the locus of morphological contact during reproduction, one would expect both natural and sexual selection to act very strongly on genitalia, and indeed they have (see William Eberhard’s underappreciated book Sexual Selection and Animal Genitalia). I suppose that because of a stigma attached to genitals, they aren’t studied nearly as much as they should be by evolutionary biologists. Here’s a video of Brennan and some of her work, first published at the xxfiles in Science.
Although biologists have concentrated on male genitalia, as those are often the most easily seen diagnostic features of related insects (that itself speaks to the importance of sexual selection, for why should genitals change so quickly compared to other traits?), Brennan also looks at the vaginas, which, being internal, are harder to see. She uses silicon molds to define their shape.
The male mako shark genitals described at 1:40 are way cool, and the spines on them probably show some kind of antagonism between male and female during copulation: the male wants to hold on to inject his sperm, but the spines don’t allow a female to reject such a male, and may damage her as well. You want more? Read about “traumatic insemination,” evolution’s version of Fifty Shades of Grey.
Brennan specializes in duck genitals, which can often be amazingly long and contorted (see one of her short videos at the Science page).
