While natural selection works operates over an individual's ability to survive, sexual selection operates over an individual's ability to mate and successfully sire offspring. In other words, sexual selection is a process through which individuals of a given species struggle to be more reproductively successful. It works in two primary ways, first identified by Charles Darwin in his 1871 book The Descent of Man and Selection in Relation to Sex. He wrote, "The sexual struggle is of two kinds; in the one it is between individuals of the same sex, generally the males, in order to drive away or kill their rivals, the females remaining passive; whilst 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." That is, sexual selection may work by making some individuals better able to outcompete other males for access to the opposite sex, or it may work by making some individuals more attractive to the opposite sex. Sometimes, both processes may be active within the same species.

Acoustic calls can be subject to sexual selection if they contain information about the caller that somehow leads to increased reproductive success. It could be that variations in the quality of a call could lead others to withdraw from aggressive confrontations, or they could simply be more or less attractive to the intended recipient. Sexually selected calls can be maintained over evolutionary time if they are "costly" to produce. For example, the tungara frog broadcasts a call that signals sexual intent to females. Unfortunately for the male tungara frog, that call is also a dinner bell for the frog-eating bat. It is in this sense that the call is costly to produce, since the male frog walks a narrow line finding sex and becoming dinner for a hungry bat. A tungara frog who is less adaptively "fit" would do better not to fake the call and become a meal, and in so doing marginally increase his potential for reproductive success. Alternatively, a sexually selected call can be maintained over evolutionary time if it is impossible to fake due to various anatomical or physiological constraints.

One such honest signal is a feature of acoustic sounds called formant frequencies, or formant dispersions, which are the "natural resonance frequencies of air in the vocal tract." In non-technical terms, formants contribute to what we might think of as vocal "quality." Formants underlie the human ability to detect differences among vowel sounds, leading to our ability to distinguish among the sounds of language. But the ability to detect differences in the formant are by no means unique to our species. Indeed, formants may provide information on the body size of a caller, at least among mammals, because there is a tight correlation between formants and the length of a caller's vocal tract, and in turn, the caller's overall body size. If larger body size is related to increased quality as a potential mate or to increased likelihood to win a fight over access to mates, and for many species it is, then the formants of an acoustic call would be a reliable way for those listening to judge the prospective caller.

Two papers in this month's issue of the journal Animal Behavior explore the possibility that acoustic signals, and formants in particular, are indicators of reproductive quality in two mammal species that couldn't be more different: the North American Bison (Bison bison) and the koala (Phascolarctos cinereus).

For Bison, Size Matters

Throughout the summer breeding season, bison bulls guard their females from other rival males through a process known as "tending." Tending consists of a set of dominance-related behaviors including postural displays, scent-marking, pawing, head-rubbing, physical fights, and vocalizations, which are known as "bellows." Four summers in a row, researchers led by graduate student Megan T. Wyman of UC Davis went to the Fort Niobrara National Wildlife Refuge in Nebraska. There, they observed a herd of 325 bison during all daylight hours, collecting a wealth of data from each male, determining the parentage for each juvenile, noting the occurrence of each copulation, and recording each mature male's bellow.

Top: Larger bulls (horizonal axis) had lower formant frequencies (vertical axis). Bottom: Lower formant frequency (horizontal axis) predicted number of copulations (vertical axis).

Together, this data allowed them to test two hypotheses. First, they determined that body mass, but not age, was predictive of the formant frequencies of male bellows, with larger bulls having lower formants. Formant frequency, then, is a reliable indicator of body mass in male American bison.

Second, they determined whether the formant frequencies were predictive of dominance, number of successful copulations, and number of offspring sired. It turned out that formant frequencies successfully predicted the number of copulations each bull had during the breeding season. Males with lower formant frequencies (and therefore longer vocal tracts) had higher mating success. While the formants did not statistically predict the number of offspring successfully sired by each bull or his position in the dominance hierarchy, the number of offspring was correlated with each of those variables. So the quality of the males' bellows may ultimately have an indirect effect on both their dominance rank as well as the number of offspring successfully sired.

Last, the researchers discovered that the bulls with high mating success had lower formant frequencies than would have been predicted by their body mass alone. This means that the highest-quality males may have unknowingly discovered a method to exaggerate the apparent length of their vocal tracts. The researchers suggest that this may reflect an "ongoing adaptation process driven by sexual selection." In the future, Wyman and her colleagues plan on using auditory playback experiments to determine whether the effect of formant frequencies on mating success is primarily driven by male competition or by female choice.

Like Bison, Like Koala

The story is strikingly similar for koalas. Postdoctoral researcher Benjamin D. Charlton of the Department of Cognitive Biology at the University of Vienna (now at the University of Sussex) and colleagues traveled to the Lone Pine Koala Sanctuary, in Brisbane, Australia. At the sanctuary, they presented sixteen adult female koalas while they were in estrous with auditory playback of bellows recorded from five different males. The researchers artificially lowered and raised the formant frequencies for each male's recordings, to approximate males with higher and lower body mass. This way they could be sure that the only acoustic variable that systematically differed among the recordings was the formant frequency itself.

The setup was quite simple. The female was placed into a small enclosure, at the ends of which were placed two speakers set to play the pre-recorded male bellows. The researchers simply noted which of two sounds the females preferred approaching.

Approach decisions were determined when the koala crossed into either of the shaded proximity areas.

They discovered that the estrous females spent more time near the sounds associated with larger males. They also looked more often, and for more time, towards the direction from which those sounds were coming.

Left: number of looks. Middle: looking duration. Right: Time in proximity zone. (Click to enlarge.)

Since there were no preferences for recordings derived from any particular male, the researchers could be sure that the females' approach behaviors were driven exclusively by formant frequencies, rather than any other possible acoustic variable. The researchers concluded that male koalas who produce bellows with lower formant frequencies would likely receive more attention from estrous females than those with higher formants, and would therefore be more likely to successfully copulate with them.

Taken together, both the bison and koala experiments suggest that variation in formant frequencies may have initially evolved through sexual selection in order to convey information about body size. Similar patterns have been observed in a wide variety of mammals, including red deer, pandas, and various primates, including humans. Given the widespread association of formant frequency with mating success in both placental mammals as well as marsupials, it is possible that these preferences emerged quite early in the evolution of the mammalian clade. This leads to a fascinating question put forth by Charlton and colleagues: since variations in formant frequency not only guide mating-related decisions, but also underlie distinctions between individual human speech sounds, what might this mean for the evolution of language?

Wyman M.T., Mooring M.S., McCowan B., Penedo M.C.T., Reby D. & Hart L.A. (2012). Acoustic cues to size and quality in the vocalizations of male North American bison, Bison bison, Animal Behaviour, 84 (6) 1381-1391. DOI:

Charlton B.D., Ellis W.A.H., Brumm J., Nilsson K. & Fitch W.T. (2012). Female koalas prefer bellows in which lower formants indicate larger males, Animal Behaviour, 84 (6) 1565-1571. DOI:

For more on vocal communication and the evolution of language:

Elephants Say Bee-Ware!

Singing Mice May Join Humans and Songbirds As Vocal Learners

Dogs Can Hear How Big You Are

Eavesdropping Iguanas Use Mockingbird Calls To Survive

Can You Hear Me Now? Human Noise Disrupts Blue Whale Communication

Babel’s Dawn: A Natural History of the Origins of Speech (Book Review)

Is Language Unique to Humans?

Images: Bison from Wyman et al. (2012); Koala by Jeremiah Blatz/Creative Commons.