Darwin Comes to Town

by Menno Schilthuizen

  What would be the effect on this theater of sexual rivalry if the medium that plays a central role is compromised by urban noise? This was the question that Hans Slabbekoorn and his colleagues were bouncing off one another around ten years ago. And, as so often with pressing academic questions, it did not take long before two PhD students were saddled with them. The first, Millie Mockford, then at the University of Aberystwyth, focused on the rival males. In twenty cities across the UK, Mockford placed a loudspeaker in the territory of an urban tit and played him a (low-frequency) song recorded outside that same city and also a high-frequency urban song. Then, she observed how the male reacted to this artificial rival. And she also did the opposite experiment: playing urban and rural songs in a rural male’s territory. What she saw through her binoculars was that the males would become much more agitated by a song that matched their own habitat. In other words, an urban tit was more offended by an urban song than by a rural song, and vice versa.

  The other study, which had a female focus, was the work of Slabbekoorn’s student Wouter Halfwerk. He discovered that urban tits face a grueling quandary. Acting pretty much like the great tit secret service, Halfwerk closely watched a population of great tits breeding in thirty nest boxes in the Netherlands. By checking these nest boxes regularly he knew exactly when the females were fertile and when they laid their eggs. DNA tests told him which chicks were fathered by the male whose territory the nest box was in. If that weren’t enough of a breach of their privacy, he also wire-tapped their homes, placing one microphone inside the nest box and another one outside. This way, he could record the male songs and also his female’s soft-voiced encouraging responses, as well as the tell-tale scratching and wing-flapping when the female left the nest box, ready for her early-morning copulation.

  What this surveillance operation told Halfwerk was that females just luuurve a deep-voiced male. The lower a male’s calls, the more likely his female was to seek his company at the moment she was expecting a new egg. Sounds romantic, but the flipside of this is that females whose male did not achieve a deep sexy song would regularly sneak out of the nest box before dawn to seek another male’s attentions. Sure enough, DNA tests showed that the high-singing males were being cuckolded: one or more of the chicks they were raising were fathered by the neighbors.

  Now, Halfwerk’s nest boxes were all in a quiet forest. To see what the effect of urban noise was, he had to add it manually. So—another secret service tactic—he subjected them to continuous noise until the tits gave up their secrets. On top of the nest boxes, he installed loudspeakers that were connected with mp3-players and pumped constant traffic noise into the poor birds’ nest boxes. Then he broadcast pre-recorded high-pitched and low-pitched male songs from a loudspeaker placed outside the box. Only when the songs were high enough to be heard over the traffic raging inside the nest box would the female emerge, expecting to be mounted by the male (but then wasn’t, as there was only Wouter Halfwerk and his loudspeaker).

  What these two studies show is that great tit sexual evolution might be on diverging tracks inside and outside the city. Their songs, the level of monogamy, and what entices a response in both males and females might all be drifting away from what is the norm outside the city. And probably similar things are happening in other urban songbirds whose voices have been cranked up a few notes.

  During this long exposé by Slabbekoorn, some of the students have decided to stretch out on the grass, while the ones still standing begin to fidget. Clearly, as far as they’re concerned, there’s only so much you can absorb about great tits, loudspeakers, song frequencies, even about early-morning copulation, and maybe it is time to consider this urban ecology practical finished. Slabbekoorn takes the hint and begins to head back to the university. But at the edge of the ditch between the poplar-lined road and the biology department, he stops for one last twist.

  “It’s not just about pitch, you know,” he says. “Urban noise can have an impact on bird acoustics in many different ways.” Australian silvereyes, for example, not only sing higher but their songs are also shorter and the musical elements are more spaced out, possibly to allow the song’s echoes against buildings to peter out—the same reason why an orator in a large stadium will speak more slowly, so as not to interfere with his own returning echoes. Robins in noisy parts of the city of Sheffield (and, one assumes, in other cities, too) sing more during the night, when it is quieter. And then there are the planes in Spain’s plains. In the flood plains of the Jarama, the dawn chorus of songbirds starts earlier where the river runs alongside Madrid airport’s runways. To stay ahead of the roar of the day’s first incoming and outgoing air traffic, the local blackcaps, warblers, cuckoos, and finches advance their internal alarm clocks by up to forty-five minutes.

  Yet there are some urban animal-sound interactions where adaptation is not possible, says Slabbekoorn. He points at the ditch behind him. “According to Dutch legislation, a building project must be shifted if a ditch would need to be drained that contains the weather loach, a protected fish species. But the piling next to that ditch will kill just as well: the transduction of sound in water is very good and also the transfer into the watery body of the fish. The piling noise will rupture fish ears or their swim bladder.” With that, we turn around and set ourselves in motion again, silent once more, but for different reasons this time.

  17

  SEX AND THE CITY

  In a suburban San Diego walkway stands a red women’s bicycle with a rusty chain, parked among a few other bikes and some gardening tools. On its rear carrier, a plastic white-and-blue child’s seat, inside which lies, upturned, a Styrofoam cycling helmet. A mother returned home on a Friday afternoon after picking up her child from school, parked the bike, and then helped her child out of the seat, who immediately wanted to run off to play in the yard. “Hey, what about your helmet, sweetie?” she would call after her, then help unbuckle the impatient child’s helmet, and cast the thing in the back of the plastic seat. But next Monday morning’s rushed commute to school was stopped in its tracks because of an unexpected turn of events: “Well, what do you know, sweetie? A birdie has made her nest in your helmet!”

  This is what I imagine may have preceded the taking of the photograph printed on page 189 of the April 2006 issue of the journal Trends in Ecology and Evolution. The reason that such a family snapshot appeared in the pages of this esteemed scientific journal is that the bird who took up residence in this San Diego shed is not just any bird. It is the dark-eyed junco (Junco hyemalis), which, in that part of North America, would normally nest exclusively in the conifer forests high up in the mountains. Until 1983, its breeding range lay hundreds of miles away from San Diego, at elevations of 1,600 to 3,200 yards. But in that year, to the surprise of local birdwatchers, dark-eyed juncos took up nesting in the coastal, urban environment of the University of California campus. Those first colonists were presumably a few mountain birds who had spent the winter near the coast, but, unlike all such winter visitors before them, decided not to migrate back up in spring. Instead, they stayed put and began nesting in the ornamental shrubbery among the campus buildings; and, yes, eventually also in bicycle helmets. Over the ensuing years, the colony grew steadily and they had reached a size of some 160 birds by 1998, the year in which biologist Pamela Yeh started studying them for her PhD.

  The birds are not much to look at: sparrow-sized, drab brown and slaty gray, with a bit of white in the outer tail feathers. But it was those white tail feathers that interested Yeh, because these play an important role in the birds’ love life. When a male junco fancies a female, he will try to impress her by hopping about, drooping his wings and fanning out his tail to display those bright white flags. In the 1990s, researchers studying the birds in their native range proved the effectiveness of this display with a simple cut-and-paste experiment. They cut off males’ tail feathers and enhanced them or toned them down by super-gluing feathers that had either more or less white on them than the original
ones. They discovered that females consistently went for the males with the whitest tails. Apparently, a male with a whiter tail, whether this is his natural color or not, makes a female junco’s heart throb.

  But why would this be so? What benefit could a female possibly gain by choosing a mate with a bit more white in a few of his feathers? Or, for that matter, with a slightly lower-pitched song, as we saw in the great tits of the previous chapter? For the answers to this intriguing question, we have to delve a bit deeper into the field of sexual selection. We’ll get back to Pamela Yeh and her urban juncos after that.

  After natural selection (where the environment selects), sexual selection (where the opposite sex does the selecting) is the second great force of evolution. Any genetic property that will make an organism sexier, and thereby gain more or better sexual partners, will see a higher representation in the next generation. As we have learned, such a change in genetic representation is, by definition, evolution. So sexual selection, as well as natural selection, will make a species evolve.

  As an example, think of the male sage grouse (Centrocercus urophasianus) with his bizarre starburst tail, white ruff, chest sacks of bare yellow skin, and tiara of plumes on his head. Over thousands of years, female sage grouse (which are plain, stripped-down versions of the male) have been most impressed by males with the greatest starbursts, whitest ruffs, most in-your-face throat sacks, and longest head plumes. Those were the ones that got to sire the females’ offspring, leaving all the less striking males without any descendants and their less-sexy genes as genetic dead-ends.

  But there is another way in which sexual selection can work. Not by active choosing by the opposite sex, but by battling among sexual rivals; the winner then takes all. Imagine male rhinoceros beetles with horns that are so big that they can topple over all their competitors and always get to mate with any nearby female. These males will pass on their big-horn genes, at the expense of the less-endowed males, and the average horn size of the beetle species will increase over time—at least until horns get so big that they become a liability (and then natural selection kicks in by removing those ridiculously-large-horn genes).

  These two examples are about sexual selection doing its thing on males. But in principle, sexual selection can work in both directions. Both females and males will select partners that seem best at producing large and high-quality litters. However, in practice, the two sexes differ in how much they stand to gain by selecting a “good” mate. In many species, the female invests a lot of time and energy in nurturing only a handful of offspring. For her, choosing the best father with the finest sperm is of the utmost importance—one wrong choice and her babies would be saddled with inferior genes. Males, on the other hand, often do not invest as much as females. For many a male, choosing the wrong female may come at a cost no greater than an ejaculate and a few wasted minutes. As a result, the evolutionary premium tends to be greatest on a female choosing the right male, and less so the other way around.

  But how do you pick a good male? First of all, the answer to that profound question depends very much on what is relevant in your particular species’ ecology. In some species, it’s important to get a male that is good at defending a territory, in other species one that is good at finding food for mother and young. And in yet another species, males do neither, and all you need from him is his sperm. Still, knowing what you need does not entirely solve the problem, because how can you tell whether a male will be a good fighter, provider, carer, or sperm-donor without actually going so far as giving him a try? What a female needs is an “honest signal”; some sort of “flag” that can be used as a proxy for a male’s true quality.

  This brings us back to the dark-eyed junco’s tail. Those stylish white rims on the male’s tailcoat are not just aesthetically attractive to females—they stand for much more. As one of Yeh’s colleagues found out, males genetically predisposed to have more white in their tails also have higher testosterone levels and are better at fighting off competing males. It is not yet clear exactly how this correlation comes about, but what is clear is that females can thereby use male tail decoration as a handy shortcut to the most testosteroney ones. In the dark-eyed junco marriage market, that is important. Up in the California mountains, the breeding season is short. The brief period during which the insects that they feed to their young are plentiful is only long enough for one, maybe two broods. That means that claiming a territory with a bountiful supply of bugs and successfully defending it against encroachment by other juncos is vital. So, what a female junco wants is a burly male who can do that. And his tail feathers will give her an important clue.

  But for the San Diego campus juncos, Yeh reckoned, life is very different. Instead of having to grapple with the limitations set by a cool montane forest, the Mediterranean climate on campus is so balmy that the birds can start nesting as early as February and, thanks to the irrigation system that negates the summer drought, keep this up throughout the summer and early autumn, raising up to four nests per year. The downside of campus life, however, is that you can be an easy target. The terrain is very open. The lawns, parking lots, and streets afford clear lines of sight for passing hawks, who regularly swoop down and snatch up a junco that ventures out into the open. So, with less need for a macho male, the urban females should evolve a taste for drabber males, while at the same time, the ones with most white on their tails would get eaten more by birds of prey. Yeh reasoned, with both these forces pushing in the same direction, the urban juncos should evolve to show less white on their tails. And, sure enough, that is exactly what she found. Compared with the mountain birds, the ones on campus had evolved about 20 percent less white. Back in 2002, that is. Has the trend toward less tail-white continued since then? Yeh: “That is a good question! We don’t know. After an extended period away from this field site, we will be sampling it come 2018.”

  Something very similar seems to be going on in—wait for it—that favorite of urban biologists’ birds, the great tit. Juan Carlos Senar of the Natural History Museum in Barcelona discovered that Barcelona’s inner city tits have narrower neckties than countryside tits. Now you have to realize that for a male great tit, the source of all his power is his necktie. The width of that vertical stripe of deep black breast feathers is mostly genetically determined and is, like the dark-eyed junco’s white tail flags, directly connected with his masculinity. Birds with broader ties are more dominant and aggressive, are better nest defenders and get to mate with better females. In other words, big tie tits are top tits.

  So why would male tits’ urban attire involve narrower neckties and thus be of the less macho kind? It could be, of course, that the city is the place of refuge that absorbs all the weaker males from the countryside that could not maintain a territory in the face of broad-tied bullies. But Senar’s work shows that that is not the case. By keeping track of the leg rings of the 500 or so males of which he knew the tie-width, he could tell how well each category survived. As it turned out, in the countryside, the broader a tie, the greater the survival—as expected. In the city this situation was reversed: narrow-tied males fared well, and broad-tied individuals were dying by numbers. So the city, it seems, has its own rules for what makes a good male.

  What the great tit and dark-eyed junco stories show is that the quality of a male in the countryside depends on different things from in the city. In these two examples, the brawler males, so able-bodied and highly-prized in the forest, for some reason seem to be less useful in the city. If so, it is to be expected that female tastes in males would evolve along with this, so that city females, too, would begin turning up their noses for those most macho of males. This would then lead to a change in the ornaments, the signals by which females gauge a male’s quality so that the birds inside and outside of cities would actually begin to look different—perhaps to the extent that they would evolve into different species, something that we will encounter in the next chapter.

  Lest the preceding pages gave you the impr
ession that the city always promotes the evolution of “metrosexual” males, there are also cases where the opposite is true. Surely you remember from previous chapters that fragmentation is one of the hallmarks of animals’ and plants’ habitats in the city. This is the case for wooded areas (think of all those small parks in New York City, where white-footed mice are marooned in a sea of mouse-unfriendly cityscape), but also for watery places. Damselflies, for example, need ponds fringed by some vegetation where they can perch, patrol for prey, and lay their eggs below the water surface. Their larvae lead lives entirely submerged, even. So for damselflies to reach and colonize the ponds, ditches, and other minuscule water bodies that dot the city, they need to fly long distances.

  Nedim Tüzün and Lin Op de Beeck, two PhD students at the University of Leuven, Belgium, figured that this need for being a strong flyer would show up in the urban ponds. They put their hunch to the test by catching nearly 600 males of the azure damselfly (Coenagrion puella), at water bodies in and around three Belgian cities, and then testing the flight endurance of each of those males in a flight tunnel. Their flight tunnel was a Plexiglas tube of two yards long and half a yard in diameter, closed at the top and placed at an angle. They would put a damselfly in a cup, release it at the bottom of the tube, and then let it fly up and away until it got tired and drifted back to the bottom of the tube. On average, the countryside damsels would tire out after three and a half minutes already, whereas the urban ones would stay aloft for more than twice as long. So, the students’ expectation was borne out: the ones that had managed to colonize inner city ponds must have been the strongest flyers, and this left its signature in the flight performance of the urban damsels.

  But what does this have to do with sex? Well, in these damselflies, the sexual game is played out primarily via competition between rival males. When they’re in the mood for love, they zigzag across the water surface and pounce on any female that shows itself. The male who reaches her first will grab her by the neck with a pair of pinchers at the end of his body and then carry her to a secluded spot for a bit of mating—meanwhile defending her against other males. For each male that they had caught, Tüzün and Op de Beeck had recorded whether it had been caught in flagrante delicto or as a lonely, unmated male. When they then checked their flight endurance data, they found that, in the urban ponds, the males that had been found in the company of a female had a flight endurance some 40 seconds greater than the ones that were netted as bachelors. In other words, in these urban insects, natural selection first makes them evolve into stronger flyers, and this is then even further amplified by sexual selection. Not only do the strongest flyers colonize the city ponds first—they also are the first to get to the available females.