[This is my third post of Sex Week]
Here’s a song for the male water strider, from the days when Rod Stewart could do no wrong:
In my first two posts for Sex Week, I wrote about the delights of courtship: the alluring, informative fragrance of yeast and the seductive buzz of electric fish. These signals stir the opposite sex into action–to creep towards a fellow fungus, or to head-butt a prospective mate. But in many species, the actual consummation that all that courtship leads up to does not turn out to be a blissful union. Instead, some males will use all kinds of force and subterfuge to prolong their mating and raise the odds that their sperm fertilize their mate’s eggs. And the females? In some species, they very often just want to get away.
The reason for this unhappy union is pretty simple. In a lot of species, males compete with each other to fertilize the eggs of females. A single male makes so much sperm that he could, in theory, fertilize every female of his species. What limits his reproductive success is the access he has to females and their eggs. Females, on the other hand, are limited by how many eggs they can produce and rear. So it can pay for them to be choosy about which males they mate with. That doesn’t necessarily mean they pick one male, however; females in many species mate with several males, and there’s evidence that they can choose which male’s sperm to fertilize their eggs.
I’ve written on the Loom before about the various forms that this sexual conflict can take, from love darts to bickering bird parents to bizarre duck genitals, but one of the most extreme cases of this unromantic behavior can be seen in your local stream. Water striders skate over the surface of water, using their legs to sense waves from their prey. When it comes time for mating, a male water strider will feel for the waves of females. He will skate–or sometimes even leap–to land atop a mate. Very often, the female will struggle to get away, but he will wrap his legs around her midsection. The two insects fight; she may try various judo-like maneuvers to get him off, while he holds on as best he can. A female may raise her metabolic rate by 200% as she battles the male. If the male manages to insert his phallus into the female’s reproductive tract, he inflates it to keep it in place. He will hold onto her as long as possible–in some cases, as long as twelve hours–to raise the odds that his sperm find her eggs, and reduce the time the female has to mate with other water striders.
This kind of behavior has evolved because it can, under some circumstances, bring male water striders more offspring. Water striders, like many animals, have different personalities. Some male water striders are aggressive, and some are hyperaggressive. They are so eager that they’ll jump on males as well as females.. A team of scientists at Binghamton University mixed together water striders with different personalities to see how they would fare in the mating game. They found that in a mixed group of males, the hyperaggressive water striders had greater success than their milder rivals.
If hyperaggressive males can pass on their genes so well, why aren’t all male water striders over the top? One reason may be that selection can have different effects on animals at different levels. At the level of individuals, hyperaggressiveness may give an edge. But water striders don’t live in isolation. They live in groups, gathering in isolated riffles or side-ponds in streams. If you look at groups of water striders, hyperaggression turns out to be a disaster for males. Hyperaggressive males wear females out with their wrestling. The females try to hide off the water, so that they can’t feed, and as a result they produce fewer eggs.
The scientists even found that females will sometimes just abandon their group and seek out another place to live, where the males aren’t so overbearing. The groups where milder males live are flooded with females, so that each male has more females to approach. As a result, groups of mellow males can have more offspring than groups that contain hyperaggressive water striders.
The battle of the sexes rages on, but the opposite effects of individual selection and group selection keep it in check.
[This is my second post of Sex Week]
In the sexual universe, all sorts of things can feel good, even if we humans have a hard time imagining how they can bring any pleasure. Electricity, for example, may be nothing for us beyond a painful shock. But for some fishes, it is the essence of desire.
The rivers and lakes of central Africa are home to a couple hundred species of fishes called mormyrids. Their tails are packed with special cells that can produce electric discharges, and they use other kinds of cells embedded in their skin to detect the field they produce. If another fish passes by them, the field becomes deformed, and the mormyrid can sense the difference.
What must it be like to be able to sense electricity this way? It’s certainly nothing like the blind pain we feel. Their specialized sensors let them sense subtle changes. They probably get a feeling that’s a bit like touch, a bit like the sensation of heat, and a bit like hearing. It’s like touch in the sense that the fishes can sense electricity across their entire body and they interpret the sensations by creating body-shaped maps in their brains. It’s like the sensation of heat in the way it is diffuse, rather than creating sharp boundaries. And it’s like hearing in the way that fishes can sense fine differences in the frequency of the electric pulses they produce.
Mormyrids are so sophisticated in their sense of electricity that they can use it to hunt in total darkness. They can scan the bottoms of rivers and lakes for hidden prey. In one experiment, German scientists tested the sharpness of mormyrid electrolocation by putting larvae under one of two shapes, a diamond and a pyramid. The fish could quickly learn to head straight for the shape with the food under it.
Mormyrids also use their electric pulses to communicate with each other. In Lake Malawi, for example, Matthew Arnegard of Cornell University and Bruce Carlson of the University of Virginia observed packs of up to ten mormyrids hunt together for smaller fishes for days at a time. The fishes sent out crackles of electricity to each other to stay in close touch as they roamed for prey.
Mormyrids have also borrowed their electric senses for a less deadly purpose: courtship. The fish have tiny eyes, and so they probably don’t care much about how attractive other mormyrids look. In the darkness of their nocturnal world, there’s not much point in putting on a fancy courtship dance or to build an attractive nest on the river bottom. Instead, mormyrids find electricity sexy.
To find a mate, male mormyrid fishes produce electric pulses, which nearby females can detect. Females don’t just rush to the first courtship pulse they detect, though. Several species of mormyrids may live in the same waters, and so if female mormyrids indiscriminately mated with any male that produced a signal nearby, the barriers between the species would soon collapse.
Instead, the females are picky. The males of of each species produce their own unique electric pulse. The photograph shown here illustrates just a few of them. In a paper with the fabulous title, “Electrifying love: electric fish use species-specific discharge for mate recognition,” German scientists demonstrated that females are attracted to the pulses made by males of their own species more than those of other species.
Females don’t just discriminate between species. They also discriminate among the males of their own species. Peter Machnik and Bernd Kramer, two biologists of the University of Regensburg, documented this female preference in a mormyrid species known as the bulldog fish. When a male bulldog fish sings his electric courtship song, an interested female will swim up to him and butt her head into his. The male will float passively, releasing more electric pulses, while the female continues to head butt him dozens of times. Then the female spawns her eggs, which the male fertilizes. (Hey, it’s a mormyrid thing; you wouldn’t understand.)
Machnik and Kramer noticed that different male bulldog fishes produced different pulses. The main variation was their duration: some bulldog fishes produced longer pulses than others. To see if that difference mattered to the females, the scietnists programmed a device to produce pulses like a male bulldog fish and put it in a tank with females. The females were so enamored by the pulses that they head-butted the device. Machnik and Kramer discovered that the females head-butted more when the pulses were longer.
Female bulldog fishes may be attracted to long pulses for the same reason that yeast like strong pheromones: it’s an honest advertisement from desirable males. When bulldog fishes produce courtship pulses, they can put themselves at risk. Catfish, which prey on the bulldog fishes, also sense electricity. If a male makes long signals, he’s putting himself at greater danger. Stronger males can afford that risk better than weaker ones.
Recently, Arnegard and his colleagues studied how these signals have evolved over millions of years. They compared a dozen different species of mormyrids from a small area of jungle in Gabon. The scientists figured out how the species were related to one another, and then they compared the mormyrids in terms of both their anatomy and their electric pulses.
They found a big difference. Even the most closely related species of mormyrids had very different signals. In fact, their signals were about as different from each other than they were from their most distant relatives at the Gabon site. Their bodies, on the other hand, evolved much more slowly. Closely related species looked more like each other than they did to their distant cousins.
This difference may say a lot about how new species evolve. The first thing that changes when two populations of mormyrids start to diverge is their electric song. The fact that individual mormyrids vary in their songs demonstrates that those songs have the potential to evolve. The electric pulses might diverge for any number of reasons. Some fishes might live with dangerous catfish, for example, while others might escape to predator-free waters where their long songs would go unpunished. Once the pulses start changing, females might evolve preferences for the new patterns. Once those preferences take hold, they will keep a population of mormyrids from mating with other fishes. The two populations would start to diverge genetically, until they branched apart into two separate species.
It may be no coincidence that mormyrids have evolved into a vast number of species–200 and probably more–while their closest non-electric relatives have only evolved into 10 species. Their electric sex lives have become an engine of biodiversity.
If yeast could sing, it might sound something like this.
This single-celled fungus–for which we should give thanks for bread, beer, and wine–can reproduce in several ways. Most of the time, it produces buds that eventually split off as free-living cells of their own. Its daughters are identical to itself, carrying the same two sets of chromosomes. Sometimes, however, life get rough for yeast, and they respond by making spores, each with only one set of chromosomes. Later, when times get better, the spores can germinate. In some cases the yeast cells that emerge just grow and divide. But they can also have sex. One yeast cell merges with another one, combining their DNA to produce a new yeast cell with two sets of chromosomes.
What makes yeast sex especially interesting is that the cells communicate with each other first. A yeast cell produces a pheromone that can cause another cell to stop dividing and start crawling towards the source of the signal. These pheromones divide yeasts into two groups. Yeast cells carry one of two genes for making pheromones and will only mate with yeast cells that produce the opposite type.
But if you surround a yeast cell with a ring of pheromone producers, the yeast will not just pick a partner at random. It will exercise a choice. The cell will measure the pheromones coming from each suitor, and it will creep its way to the strongest source.
Some scientists have suggested that natural selection favors this choice because it lets yeast be efficient about sex. Rather than creep a long way to find a mate, a yeast cell can just love the one it’s with. But there are some problems with this explanation.
First off, yeast make a lot of pheromones–much more than they would need simply to be detected. For another thing, yeast cells vary in how much pheromone they make. A strong pheromone maker will be more likely to attract a mate than a weak one that’s closer. What’s more, when a pheromone-producing yeast cell detects a signal from the opposite mating type, it cranks up its own signal. If you didn’t know better, you might think yeast cells were trying to get some attention.
In fact, some scientists think that yeast are doing exactly that. They argue that yeast cells release pheromones like a love song, in order to attract mates.
Carl Smith and Duncan Greig, two evolutionary biologists at University College London, wondered if the same pressures drove the evolution of yeast pheromones that have driven the evolution of more familiar kinds of sexual displays, like peacock tails, frog croaks, and elk horns. According to one particularly influential hypothesis, the Handicap Principle, females could benefit from being choosy about mates if that choice led them to have more success reproducing. Of course, a male frog can’t offer a female frog a DNA test documenting his good genes. So he needs some way of advertising his quality. A song or a horn or a fragrance are all possible ways to send this signal.
The problem with this sort of communication is that it can be hacked. A weak male can, in theory, channel some extra energy into building a false sexual display. If some males start to cheat, females who are choosy will end up with no advantage over other females. Female choice will disappear, and male displays will vanish as well.
Honesty is thus crucial to the evolution of sexual displays. And one way for displays to be honest is for them to be expensive. A weak male with fewer resources will have a harder time producing an expensive display than a strong one. In effect, a long-tailed widowbird is saying, “I’ve got so much to offer that I can waste a lot of energy on these magnificent tail feathers.”
To see if yeast were wooing each other with expensive signals, Smith and Greig disabled the genes in some cells so that they could not make pheromones. Then they compared how fast healthy and engineered yeast cells reproduced asexually. The quiet yeast grew far faster, the scientists found, presumably because they no longer had to use up a lot of energy making pheromones. This result confirmed a key prediction of the handicap principle: a signal has to be costly. In fact, yeasts can suffer a 30% drop in their viability by making pheromones.
But some yeast pay a bigger price than others. Some strains of yeast Smith and Greig studied carried mutations that caused them to grow relatively slowly, while other cells could grow faster. Smith and Grieg found that when they disabled pheromone genes in low-quality yeast, the cells enjoyed a much bigger boost than high-quality yeast. In other words, making pheromones is a bigger sacrifice for low-quality cells than for high-quality ones. That difference could help ensure that pheromones remain an honest signal.
Finally, the scientists compared how much pheromones each kind of yeast produced. They found that yeast of higher quality churned out more pheromones than yeast of lower quality. So a yeast that chooses to mate with a strong pheromone producer will be endowing its offspring with good genes.
Smith and Greig’s experiment makes me think about the yeast in a glass of wine in a different way: I now imagine an ocean of love songs. But it also makes me appreciate just how far-reaching Darwin’s ideas about the evolution of sex have turned out to be. The same rules apply–to bird, frog, and fungus alike.
Birds do it, bees do it, even educated viruses do it. And for some reason my stack of interesting scientific papers is particularly heavy at the moment with research on the evolution of sex. So let’s not be shy. All this week, I will blog about sex.
[Image: mating sand wasps, Alex Wild]