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  Either way, the rare-male effect might also lead to the kind of evolutionary dynamism I mentioned above. And again, it has required a theoretical biologist to fully reveal this for us. Hanna Kokko, a Finnish theoretician at Australian National University (known for the mysterious haikus with which she summarizes her research projects on her home page: “Bird here, two out there / Eggs in baskets wet or dry / Covariances”), has been the first to run computer simulations of the rare-male effect. Her work revealed that in a population of, say, guppies, where several color types of males exist, as well as a rare-male effect in the females, the genes for different male colors will keep fluctuating in frequency over time.

  This is because a rare type of male will, as time goes on, initially become more frequent as it enjoys female preference. However, in this success lies its downfall, for the commoner the male type becomes, the less it will be considered sexy by rare-male-preferring females. Eventually, female attention shifts to the next rare kind of male. At the same time, the genes that make females prefer rare males are also prone to such fluctuations: whenever these genes increase in the gene pool, rare male types will rise to commonness in just one generation, rendering their offspring unattractive for not being a rare type anymore. And since these offspring also carry their mothers’ preference in them, these genes, too, will decline in the next generation.

  What the computer simulations of guppy color as well as the sexiness of fly eye length show us is that when male signals and female preferences evolve in a species, there may be feedback loops that could cause unpredictable patterns. Like weather systems, where humidity, air pressure, and sunlight all conspire to drive chaotic cycles of rain and shine, the evolution of seduction is full of unpredictability. Imagine that you have a set of identical animal species and let sexual evolution run its course in each of them. It would be like setting up a number of PCs and letting each of them run a simulation program written by Kokko or Pomiankowski. Even if the initial conditions (the population sizes, the length of a generation, and the kinds of genes responsible for signals and preferences) are precisely identical at the outset (which in nature they will never be), the random effects of demographics and genetic mutation will cause these runs to branch out in different directions in just a short span of time. When the simulations are over, the sexual signals and preferences in each species—initially identical—will have drifted apart beyond recognition.

  Now substitute genitalia for color patterns and eyestalks. If sexual selection on genitalia indeed progresses in a similar fashion, as Eberhard believes, then evolution will be like a fickle sculptor with ever wet clay, molding genital shape in continuously changing shapes and forms, never satisfied, never allowing it to set. And with such rapid and erratic evolution, it is no wonder that different species have such different genitalia, since each is just a snapshot of that ongoing dynamic interaction among genetic mutation, sensory drive, and female choice.

  But it is easy to get carried away by computer simulations and fancy evolutionary theory. Is this really what goes on out there in the wild world of real animals with real genitals? What do we see when we try to watch genital evolution in action? Time for a reality check.

  Look Back in Amber

  Observing ongoing evolution of genitalia in the real world is not easy. Other organs and body parts have been seen to change shape in wild animals over periods as short as a few decades (the beaks of Darwin’s finches in the Galápagos Islands, for example), but as far as I know, nobody has accomplished the same with genitalia. Fortunately, paleontology provides us with the next best thing: a peek into the procreative past.

  As Australian geologist John Long explains in his 2012 book The Dawn of the Deed, the paleontology of sex is still in its infancy—a fact largely due to the puny likelihood of sexual organs, let alone sexual behaviors, fossilizing and making it to museum drawers. There are a few exceptions, and Long describes them lovingly. Like the three-hundred-million-year-old pair of sharks from a Montana sediment, one biting the head spine of the other, a preliminary to shark sex (sadly, in this case, never consummated). Or the famous fossil pit site of Messel, in Germany, which has yielded many petrified mating pairs of turtles, each couple cemented in eternal embrace. And Long himself has been instrumental in the discovery of the world’s oldest pregnancy and umbilical cords in so-called placoderm fishes from the Devonian, 380 million years ago, and working out the mechanics of their copulation and reproduction.

  Less ancient, but much better preserved, are those insects caught in the act by a clear drop of ancient pine tree resin, hardened into the famous twenty- to forty-million-year-old amber of, for example, the shores of the Baltic Sea or the Dominican Republic. Prized pieces in collections of insects in amber often contain entombed mating pairs of fungus gnats, scavenger flies, or mites. And the nice thing about these insect copulas is that they are not just hollow shells; the genitalia that once were central to their erstwhile sex lives still reside, often perfectly preserved, inside the amber sarcophagus. The only problem is that in order to study those internal organs, the valuable specimen needs to be destroyed. You’d think. But Michel Perreau, a physicist/entomologist at University Denis Diderot in Paris, has found a way to take a peek at those genitalia without needing to crack the specimen.

  Using a technique developed for medical imaging at the particle accelerator of the European Synchrotron Radiation Facility in Grenoble, Perreau managed to make high-resolution CT scans of a tiny beetle in Baltic amber. Because the synchrotron radiation does to X-rays what a laser does to visible light, it gives images with high contrast and a resolution down to a thousandth of a millimeter (0.0004 inch). So Perreau was able to get three-dimensional pictures of the genitalia of the less than 2-millimeter-long (0.1-inch) insect without as much as scratching the surface of the prized amber object. Not that it was a breeze—to do his virtual dissection, Perreau had to tell the computer for each individual detail, sometimes even pixel by pixel (or rather, voxel by voxel, the 3-D equivalent of a pixel), which parts belonged to the genitalia and which did not. “Very much work!” he sighs at the memory of the many days spent behind the keyboard. Still, in the end, what he had on his computer screen was a detailed 3-D rendering—a so-called microtomograph—of a forty-million-year-old, 0.4-millimeter-long (0.016-inch) beetle penis, which he could flip and rotate and inspect from all angles at the click of a mouse button.

  The digital ancient aedeagus showed that the beetle belonged to an ancestral species of Nemadus, a kind of Northern Hemisphere beetle that scavenges detritus in bird nests. Still, it was clearly an unknown extinct species (which Perreau good-humoredly named Nemadus microtomographicus) with a penis shaped differently from all present-day species. Since then, Perreau has brought back to life a few other beetle penises, all distinctly different from the ones sported by their current descendants.

  Still, stunning as these amber aedeagi might be, there are simply not enough of them to really reconstruct the history of genital shape and function. What we need is insects of the same family or the same genus represented in amber of a whole range of different ages, so that the changes can be tracked in time. But there are only a few places in the world where good-quality amber comes to the surface, and the amber found in one place is usually of more or less the same age. For most kinds of insect this results in three or four time slices at best. So attempts to use amber insects as an archive of evolutionary changes in genitals are frustrated because, as is so often the case with fossils, they are too few and far between.

  A much richer source of information is the insect remains that are often found in peat deposits, where they are preserved in perfect condition because of the absence of oxygen in such environments. Though younger than amber insects—they mostly date back to somewhere within the last half a million years or so—peat fossils come in much larger numbers, especially beetles with their tough, decay-resistant outer armor. The late Russell Coope was a legendary British paleonto
logist who made those peat beetles his bread and butter, routinely using their preserved genitals to identify the species. In the 1970s he studied a mother lode of 43,000-year-old beetle fragments from the Thames valley in England, consisting of thousands of specimens of almost three hundred different species. And whenever he came across a beetle abdomen, he would extract the genitalia and make perfect microscope mounts of them to compare them against identification keys for present-day species.

  The curious thing is that Coope rarely found any sign of evolutionary change in the beetle genitalia, not in the Thames valley specimens or in much older specimens. In a 2004 paper in the Philosophical Transactions of the Royal Society, he vents his surprise about this: “[A]lmost all fossil specimens match precisely their modern equivalents. These similarities even extend to the intimate intricacies of their male genitalia, which can be dissected out of compressed abdomens frequently found in the fossil assemblages.”

  Now this is a bit of a puzzle. We know that closely related species of beetles often have wildly different genitalia, so these must have changed at some point during or after the splitting up of species. And theory tells us that genital evolution should be particularly fast and dynamic. Yet Coope’s fossilized beetle penises tell a different story: they speak of stability instead. Of course, there are ways to solve Coope’s conundrum. First of all, most of the fossil beetles he studied are just a few tens or hundreds of thousands of years old—perhaps too short for the really big steps in genital evolution. And also, Coope never performed any accurate measurements on the shape of the genital organs. He simply observed that he could use the ancient genitalia to identify their owners as present-day species; small differences may have evolved during the millennia that elapsed since his specimens were alive, but these may have been too small for Coope to notice.

  On the other hand, it could also be that Coope uncovered a true aspect of genital evolution, and that these organs do not evolve in a smooth ebb and flow of continuous change, but in fits and starts instead. Whether evolution is usually gradual or erratic is a more general debate in evolutionary biology. There are some, like the late Stephen Jay Gould, the famous Harvard University paleontologist, who maintain that evolution tends to be concentrated in short periods of quick change, interspersed with long periods of stability—a pattern named “punctuated equilibria” by Gould (and “evolution by jerks” by his critics). The alternative is gradualism: smooth, continuous, imperceptible change all the time. This is what Darwin envisaged when he wrote, “We see nothing of these slow changes in progress, until the hand of time has marked the lapse of ages” (and which Gould, with inimitable wit, called “evolution by creeps”).

  Fortunately, over the past decade or so, scientists have come up with methods to measure whether a particular feature evolves by jerks or by creeps. To do this, you first need an evolutionary tree based on DNA. DNA is made of long strings of four different chemical compounds (the names of which are abbreviated to the familiar A, C, G, and T), and it evolves over time by accumulating mutations—chemical changes in which one or more “letters” are replaced by other “letters,” or are lost or multiplied (see Chapter 1). Since these mutations take time to happen, you can use the amount of shared “letters” in the DNA of two species to determine how close they sit together in an evolutionary tree: the fewer differences, the more recently their common ancestor split up. (The techniques are much more sophisticated than that, but basically this is what it boils down to.) So, using the information contained in DNA sequences of a group of species, evolutionary biologists can draw up an evolutionary family tree for them, which can be read from bottom to top as the order and timings of splits of ancestors into descendant species over time.

  Mark McPeek of Dartmouth College in Hanover, New Hampshire, employed such DNA-based trees to figure out how reproductive organs evolve in Enallagma damselflies. Some forty species of these pretty, dainty, blue-and-black damselflies (also known as bluets) occur all over North America, Europe, and northern Asia, and back in 2005 scientists had already used their DNA to work out the exact evolutionary tree for all of them. What McPeek and his team did was study how the shape of the male damselfly’s apparatus of claspers at the end of his abdomen changes along the branches of this family tree.

  These tongs-like organs are not strictly speaking genitalia, because of the peculiar way in which damselflies mate. Males hang around ponds waiting for females to arrive from their foraging trips. Once a female is spotted, a male will literally pounce on her in midair and grab her on the neck with those claspers he has. Then he releases a small droplet of sperm from an opening just in front of the claspers and, without releasing the female, bends the tip of his long abdomen forward to transfer this sperm droplet to his actual penis at the base of his abdomen. If the female decides to accept as a mate the male that is holding her, she will, while still dangling beneath him, bend her abdomen all the way forward to make her genitalia meet his and receive his sperm (more on this weird mating system in Chapter 6).

  Now, those male claspers differ a lot among species, which McPeek documented by creating 3-D images of them in a CT scanner. Then he used the same sort of software that computer animators use, to work out mathematical formulae that accurately reproduce the three-dimensional shapes of the species-specific claspers. These formulae then gave him a way to measure the differences in shape: the more terms and parameters were different between the formulae for a given pair of species, the more different their claspers had to be. Finally, he compared these measurements against the DNA tree and was surprised to find that there was no relation between the degree of clasper difference between two species and the time since the two species had last had a common ancestor. Old species were no more different than young species. This meant that each species had experienced only a single “jerk” of clasper evolution, rather than a slow process of gradual change. Similar signals of evolution by fits and starts have been found in the genitalia of cactus flies and millipedes.

  These results—the fossil evidence as well as these tree-based analyses—demonstrate that, despite rare-male effects and Pomiankowski’s sexual tango, there appear to be certain glass walls that limit the kinds and amounts of change that are possible and sometimes cause genital evolution to get stuck in a rut. In that sense, genitals evolve sometimes jerkily, when a new female fad evolves, and sometimes creepily, when it inches closer to one of those glass walls. So we need to adjust our image of genital evolution a little bit: although it does often spiral out of control, rapidly generating extravagant shapes and bizarre forms, it can sometimes also be constrained in an evolutionary straitjacket. In the next section, we’ll meet a few such constraints: ways in which genital evolution in certain animals is capped.

  Size Does Not Matter

  Nobody seems to know exactly where the (much overrepeated) phrase “Size doesn’t matter” was first uttered, but its roots lie in the famous sex studies of Masters and Johnson of the 1960s, in which they write, “Another widely accepted ‘phallic fallacy’ is the concept that the larger the penis the more effective the male as a partner in coital connection.” Whether penis length is particularly valued by women or not is a matter of intense and seemingly endless debate in the glossies and scientific journals alike (remember the relation between penis length and vaginal orgasms in Scotland from Chapter 4). But in a zoological sense, average size, rather than extreme size, appears to be at a premium—in humans as well as in other animals.

  This has to do with phenomena called isometry and allometry, which are the case when body measurements do or do not scale in proportion, respectively. People with bigger bodies tend to have bigger livers, for example, and for every step increase in weight, you’ll find an identical increase in liver weight; somebody who weighs in at a hundred kilos will have a liver twice as heavy as somebody of fifty kilos. So livers are said to have an isometric relationship with body size (isos meaning “same” in Greek). But if you take a different organ
—say, the brain—you’ll find allometry (allos meaning “different”) instead: heavy, big-bodied people do have bigger brains than smaller people, but the difference in brain size is much smaller than the difference in body size. Such organs, which seem to hover around the same size no matter what happens with the size of the rest of the body, are called negatively allometric. (Positive allometry also exists—the long bones of our arms and legs are disproportionately longer in taller people than in shorter people.)

  Now it is a curious rule in nature that genitalia show allometries that are about as negative as they get. Take the stag beetle Lucanus maculifemoratus, or miyama-kuwagata, as this stunning rusty black beetle is lovingly called in its native Japan (where big beetles like these are routinely kept as pets and department stores have special “insect care” sections). Entomologist Haruki Tatsuta caught forty-seven males—characterized by their gigantic antler-like jaws—in oak forests in Hokkaido and then (perhaps somewhat less lovingly) cut them up into four separate pieces: head with jaws, thorax, abdomen, and aedeagus. Each part he dried in an oven and then weighed. What Tatsuta found was that whereas the dried body of the biggest beetle was ten times as heavy as that of the smallest, his penis was barely one and a half times heavier. Compared with body size, but also with the sizes of separate body parts, the beetles’ genitalia showed strong negative allometry.

  Stag night. Stag beetles and their penises (shown below each beetle) display so-called negative allometry: no matter how large each individual animal is, stag beetle genitals are always nearly the same size.