Much of what we know about vocal learning and memory in people comes from our studies of songbirds. Each songbird species sings a distinctive song that functions as an acoustic signal for identifying species and maintaining species barriers.
In many species of songbirds, young birds learn their songs and acquire their song preferences by imprinting on the songs of nearby adult males. But some of the songs that nestlings are listening to are sung by other songbird species who also live nearby. Why don’t nestlings imprint on the songs of other songbird species?
We’ve long known that young songbirds recognize songs produced by their own species and by closely-related species (i. e., ref; and see Figure 1):
You might think that when two closely-related species live in the same area, hearing the song of the other species would erode the reproductive barriers between the species, yet nestlings can still accurately discriminate and selectively learn their own species’ songs. These abilities indicate that songbirds’ sound perception abilities are truly exceptional, even at the earliest stages of development. Nonetheless, the mechanisms underlying early song discrimination remain unknown.
Currently, we’ve identified a variety of factors that influence early song discrimination in songbirds (Figure 1a & b). For example, early acoustic experiences are important: we know that some species learn their parents’ songs and calls whilst they are still embryos in their eggs (ref), and after hatching, they must then produce an appropriate call before their parents will feed them (ref).
In addition to early acoustic experiences, other factors are known to play a role in song discrimination, including maternal effects, particularly testosterone deposited in egg yolks. This, in turn, influences neural development.
Genetics also plays a critical role, especially in discrimination between songs of closely-related species. But it is difficult to convincingly tease apart the influence of genetics from early acoustic experiences and maternal effects.
The authors of a hot-off-the-presses study, behavioral ecologist David Wheatcroft, a postdoctoral fellow, and his advisor, Anna Qvarnström, a professor in the Department of Ecology and Genetics at Uppsala University, designed an exceptionally lovely series of experiments to accomplish just this.
Nestling song preferences do not depend on early song experience
The collared flycatcher, Ficedula albicollis (video above), and the European pied flycatcher, Ficedula hypoleuca (video below), are ideal study species for this research because they inhabit partially overlapping ranges in portions of central Europe, and because they are sister species — each other’s closest living relatives (ref).
The males of these two species can be visually and auditorily identified, whereas the females and juveniles cannot be. These migratory species nest in tree cavities and feed primarily on insects and arthropods. When these two species are found side-by-side, like they do on the Baltic island of Öland where the study populations reside, the pied flycatcher will either sing “mixed songs” that contain elements from collared flycatcher song or they will mimic collared flycatcher songs. Every once in awhile, they hybridize. In this case, mistakenly choosing to mate with the wrong species is a disaster, evolutionarily speaking, because these hybrids are sterile.
These two species’ songs sound similar but they are different enough that even humans can distinguish them. More importantly, the acoustic differences in their songs are crucial to these birds for maintaining species-specific mating patterns (sonograms, Figure 2a):
Dr Wheatcroft and Professor Qvarnström began their experiments by measuring the responses of nestlings raised by parents of their own species to recorded calls of the same species (“conspecifics”) or to recorded calls of the other species (“heterospecifics”). As you would expect, they found that nestlings responded most strongly by begging and moving around when they heard recorded playbacks of conspecific calls (Figure 2b).
When eggs were swapped to the nests of the other species for incubation and rearing, the researchers found that the fostered nestlings still responded more strongly to conspecific calls (grey panel, Figure 2b) despite having no previous experience hearing their own species’ songs. Thus, early song discrimination in these species does not depend on the nestlings’ early acoustic experiences.
Nestlings’ early song preferences are genetically determined
Song preferences can depend upon species-specific maternal effects, such as the deposition of hormones into yolk. If these birds’ song preferences depended upon maternal effects, then the nestlings will respond most strongly to the songs of their biological mother’s species, regardless of their father’s species.
To test this possibility, Dr. Wheatcroft and Professor Qvarnström hybridized the two flycatcher species and repeated their playback studies with the hybrids. They found that the hybrid nestlings responded most strongly to pied flycatcher songs, regardless of which species their mother was (Figure 3):
This is opposite to the pattern that would be expected if maternal effects underlie song discrimination. But this is exactly what you would expect if early song discrimination is genetically determined (Figure 3a). Additionally, this experiment shows that pied flycatcher song preference is dominant to collared flycatcher song preference since this trait always shows up in the first generation (F1) of hybrids.
Genetic song preferences can play a pivotal role in the formation of new avian species
“Our study is the first to demonstrate that song discrimination depends on genetic differences across species,” said Dr. Wheatcroft in email.
A genetic basis for early song discrimination in songbirds has wide-ranging consequences for how species-specific mating signals and preferences can be established and maintained, even when sister species live side-by-side.
“This shows that something built-in to the genome influences the perception of sounds in a remarkably specific way, since the songs of both species are relatively similar.”
Considering the close genetic relationship between European pied flycatchers and collared flycatchers, these genetic differences can arise over very short time scales in wild birds.
Interestingly, Dr. Wheatcroft and Professor Qvarnström found that female hybrids tended to show stronger song discrimination than male hybrids. These findings are consistent with previous studies and suggest that song discrimination ability in male and female songbirds is controlled by a similar set of neural mechanisms and genes.
“[T]hese results suggest that these genetic differences should help prevent young songbirds from learning the songs of closely related species,” Dr. Wheatcroft explained. Such genetic differences ensure that nestlings learn their own species’ songs and that they mate with their own species as adults.
“This should help maintain reproductive boundaries across species and may even be an important factor in the formation and maintenance of new species.”
David Wheatcroft and Anna Qvarnström (2017). Genetic divergence of early song discrimination between two young songbird species, Nature Ecology & Evolution, published online on 12 June 2017 before print | doi:10.1038/s41559–017–0192
Douglas A. Nelson and Peter Marler (1993). Innate recognition of song in white-crowned sparrows: a role in selective vocal learning? Animal Behaviour 46(4):806–808 | doi:10.1006/anbe.1993.1258
Diane Colombelli-Négrel, Mark E. Hauber, Jeremy Robertson, Frank J. Sulloway, Herbert Hoi, Matteo Griggio, and Sonia Kleindorfer (2012). Embryonic Learning of Vocal Passwords in Superb Fairy-Wrens Reveals Intruder Cuckoo Nestlings, Current Biology, 22(22):2155–2160 | doi:10.1016/j.cub.2012.09.025
Diane Colombelli-Négrel, Mark E. Hauber, and Sonia Kleindorfer (2014). Prenatal learning in an Australian songbird: habituation and individual discrimination in superb fairy-wren embryos, Proceedings of the Royal Society of London B: Biological Sciences, 281:20141154 | doi:10.1098/rspb.2014.1154
Krystyna Nadachowska-Brzyska, Reto Burri, Pall I. Olason, Takeshi Kawakami, Linnéa Smeds, and Hans Ellegren (2013). Demographic Divergence History of Pied Flycatcher and Collared Flycatcher Inferred from Whole-Genome Re-sequencing Data, PLOS Genetics, 9(11):e1003942 | doi:10.1371/journal.pgen.1003942
Enjoy my writing? Please give me a few handclaps to recommend this piece. Follow me on Medium for more like this.
.. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. ..
Originally published at Forbes on 13 June 2017.