Behavioral work on many animals, ranging from insects to mammals, has shown that females prefer a certain type of male call: perhaps one that is longer, louder, or has certain combinations of sounds. We’re not sure why these preferences have evolved, though there are many theories. Those include hypotheses that males with, say, louder calls are healthier, and would confer better genes on their offspring, or that the calls are species-specific and a narrower “call window” prevents you from mating with another species and producing maladaptive offspring. The phenomenon of mate preference in females is well documented, but its evolutionary basis is poorly understood—such studies are very difficult. How can we learn what a female gains by mating with one kind of male versus another? Those studies must be done in the lab, and involve tricky preference tests combined with accurate measurements of female offspring number and quality.

Mike Ryan’s group at the University of Texas in Austin has spent years studying mating behavior (and how it relates to male calls) in túngara frogs (Engystomops pustulosus), a species found in Mexico and Central and South America. Males sit in or near streams and croak for hours, hoping to attract females with the beauty of their calls.

In most cases, female túngara frogs prefer male calls that are more complex, louder, and have lower frequencies and faster call rates, though the situation is complex. (One possibility for the louder-call preference is that those calls are producer by larger males, who not only can fertilize more eggs but may have better genes. They thus could confer a non-genetic benefit on the female (more sperm means more offspring) or a genetic one (offspring carry their father’s genes that make the sons bigger and themselves more likely to get mates).  Both advantages could, over time, impose natural selection on females to prefer certain kinds of calls.

Below are some videos, audio clips, and photos of male túngara frogs calling. As you see, males put a lot of energy into attracting mates, using both their bellies and inflated vocal sacs:

Males calling:

(See also the video at the bottom of the Science News blurb.) If you click on the screenshot below, you’ll go to a page where you can listen to a typical call: a loud squawk followed by a series of “chuks,” which increase its complexity:

Calling has its dangers, too. Males who emit more elaborate calls are subject to more predation by fringe-lipped bats, who presumably can detect the frogs more easily. That counterselection may prevent males from evolving even more elaborate calls, for there might be a point beyond which the higher predation outweighs the advantage of attracting females. Here’s a calling male meeting a sad fate (photo by Christian Ziegler from Smithsonian.com):

One thing that’s tacitly assumed in studies of mate preference is that there is a continuum of call characteristics that is fixed and transitive. That is, if call A is preferred over call B, and call B over call C, then call A should be preferred over call C.  And the order of preference shouldn’t change if other calls are present in the population. But a new paper in Science by Amanda Lea and Mike Ryan (reference and free download below) shows that this might not be the case, at least in this frog.

Their hypothesis was that “decoy” calls could actually change the order of preferences between two calls, making the least preferred call the most preferred. They tested this by making three artificial calls of differing attractiveness to females, and then testing the females’ preferences by playing these calls through speakers in the lab, seeing which speaker a female hopped toward.  (Directional hopping towards a sound source is a common way to estimate female preferences in frogs.)

Lea and Ryan based their experiment on a human analogy: psychological preferences can change direction when a decoy preference is thrown into the system. Here’s how their paper describes the “decoy effect”:

One well-known violation of regularity is the “decoy effect”. For example, while shopping for a used vehicle, the buyer may value both low price and fuel efficiency. Of the two vehicles considered, one has a higher price tag but also better efficiency (A), whereas the second has a lower price but also lower efficiency (B). The buyer decides that he or she values lower prices over higher efficiency and so chooses B. At this point, the salesperson mentions that there is a third vehicle (C), which also has good fuel efficiency but a much higher price than both A and B. This causes the buyer to reconsider, despite no interest in the higher-priced vehicle. To the salesperson’s delight, the buyer ultimately chooses A, spending more money for better fuel efficiency. This irrational behavior has been produced by the decoy effect.

Do frogs do the same thing with calls? Lea and Ryan made three artificial calls differing in “type” (presumably complexity) and rate. The call most preferred in choice tests was call B, with call A significantly less preferred. Then they made a really lousy call, call C, which served as the decoy call, When pairs of calls were tested, B was more preferred than A, and both were preferred more than C.

The twist was then giving individual females a choice of all three calls presented simultaneously. And they did this in two ways. First, they put speakers on the floor emitting all three calls at the same time, and seeing which one the females chose (A below). Then they put the decoy call (C) on a ceiling-mounted speaker, so the female could hear it but not “choose” it, as she couldn’t hop to the ceiling! That’s design B below.

And here are the results, shown as the proportion of frogs choosing either A (light gray) calls or B (dark gray calls) in two situations: the “binary” (the decoy call not broadcast), and “trinary” (decoy call broadcast).  The top plot below is from design A above, when the “trinary” situation involves females being able to hop toward the decoy speaker (those preferences aren’t given). The bottom plot is from design B, where females could hear the decoy call but not “prefer” it by moving toward it. Again, the data are just the relative preferences for A and B.

Let’s look at the top figure first (C; it’s a bit confusing because the figures are given designations that use the same letters as call type). When calls A and B are tested against each other without the decoy call, B is slightly preferred (as it was in the preliminary experiments), but the difference is not significant. However, things change when the decoy call is played: all of a sudden call A becomes strongly and significantly preferred (asterisk shows statistical significance, with a p less than 0.05). The decoy has altered the preference, but not reversed it since there was no significant preference between calls A and B in the “binary” experiment. The alteration, as shown by the comparison with three asterisks between the binary and trinary experiments, is highly significant (p < 0.001).

The results are similar, but even more striking, in experiment B, when the decoy call was played from the ceiling. In this case when only A and B were played, there’s a strong and significant (p < 0.05) preference for B, as in the preliminary experiments. But when the decoy was played from the ceiling, all of a sudden females significantly preferred call A (p < 0.05), a reversal that was significant when binary and trinary tests were compared (three asterisks: p < 0.001).

In both cases, then, throwing a third “decoy” call into the mix makes female prefer a call that was either neutral or less preferred when tested against one alternative call. In other words, the direction of mate preference was not fixed, but altered by a third call—a call that was the least attractive!

What’s the upshot? Clearly, in this experiment (and we’re not sure if the same results would occur in nature rather than the lab), mate preferences are not fixed but malleable: they change depending on what other calls abound in the environment. What we see is similar to the “decoy” effect described by Lea and Ryan for car-buying, with call C playing the role of the more expensive, gas-efficient car.

But what does that mean? First of all, we don’t know whether the result is a general one: is this intransitivity typical of animal mating systems? The authors cite one or two papers suggesting this may be the case in some other species (I haven’t read them), but we’d need a lot more experiments like this to see how general the “decoy” effect is in nature.

But why does this happen at all? Does it make any evolutionary sense, or does it simply reflect confusion on the part of the females, who are thrown off by the decoy call? But if that were the case, why would their preference all of a sudden switch to the suboptimal call A?

We don’t know, but at the end Lea and Ryan suggest some hypotheses:

In socially complex situations such as frog choruses, rational decisions could be time-consuming, potentially resulting in lost mating opportunities or the risk of further exposure to predators. Decision rules might evolve to include loss aversion, mitigating the risk of costly errors, which are more likely when there are extreme alternatives and in uncertain environments. Such heuristics could lead to stabilizing selection on male traits and maintenance of genetic variation. Moreover, as human consumers are susceptible to manipulation by salespeople, context-dependent choice rules may make female frogs vulnerable to behavioral exploitation by competing males; for instance, if males are selective of their nearest neighbors.

Although it is clear that female choice patterns do not coincide with the consistent valuation predicted by traditional models in sexual selection, it is far from clear whether perfect formal rationality is mutually compatible with optimal evolutionary fitness. Closer inspection is required to determine whether inconsistencies revealed by decoy effects are, in fact, suboptimal in the context of fitness maximization. Variation of female mate choice in different social contexts might reflect adaptations for using additional sources of information, resulting in the expression of more complex but predictable choice patterns.

What they’re saying here, in scientific jargon, is that this might just be an irrational mess without adaptive significance. (Perhaps call B just comes through more clearly than does call A when the decoy call is played.) But they also propose alternative scenarios, involving spatial proximity, predators, and loss aversion—all of them adaptive. That is, the changes in preference in the presence of a third call could be an evolutionary phenomenon that gives the female higher offspring number.

Such adaptive hypotheses might make sense, but not necessarily in light of the decoy results. For example, if females want to avoid long-distance hopping, or predators, by mating with the nearest caller rather than the most attractive, that does make adaptive sense, but doesn’t seem to relate at all to Lea and Ryan’s result that the presence of a decoy call makes the female reverse her preference. Why the reversal? And perhaps it’s adaptive to just mate with any male when the acoustic environment is confusing, but again that fails to explain the switch in preference rather than just a loss of preference.

In the end, I find the experimental results intriguing, but their meaning unclear. That’s not the experimenter’s fault, for although they expected decoy effects, their significance, and whether the explanation involves adaptation, would be very hard to disentangle. The only problem I have with the paper, and it’s a minor one, is that the adaptive hypotheses don’t seem to relate very well to the experimental findings of a reversal of preference. What is sound (pardon the pun) is the finding that relative preferences between two call types can be dramatically altered by the presence of a third call.

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Lea, A. M. and M. J. Ryan. 2015. Irrationality in mate choice revealed by túngara frogs. Science 349:964-966.