Song lines
Natural History, Sept, 2006 by Robert B. Payne, Michael D. Sorenson
Assailed by the piercing, seemingly nonstop demands of a wailing newborn, what mother has not wished, at least for a moment, that she could outsource her childrearing to some kind neighbor? Wouldn't it be nice to fly off for a week, a month--forever--to reclaim freedom, silence, and perhaps even romance? Indigobirds are living this fantasy.
They are also providing biologists with another good example of what Stuart Bearhop is describing among European blackcaps in his article, "Change in the Air": the process of sympatric speciation, in which one population of animals splits into two species in the same geographic location.
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Ten closely related indigobird species, all native to Africa, consistently lay their eggs in the nests of other birds, mostly firefinches. Then they take off--saving themselves the hassle of foraging for food for their young and freeing themselves to breed again. The firefinches, meanwhile, raise the indigobird young along with their own chicks in the same nest.
Why doesn't the firefinch parent kick the intruders out of her nest? Even among people, it would be the rare neighbor who would put up with your kids forever without making a squawk. For one thing, when indigobird chicks open their mouths to beg for food, the firefinch mother sees an intricate pattern of black, blue, yellow, and white stripes and dots that, through natural selection, have evolved to look indistinguishable from those of her own chicks. The indigobird chicks also mimic the movements, and, in some species, the begging calls of the host's own chicks.
Yet surprisingly, our observations show that firefinches are not always duped by such evolutionary disguises. When food is in short supply, firefinches may remove the interloper's egg, which differs in size from her own. But when food is plentiful, firefinches raise the indigobird chick. The apparent selflessness of the firefinch may actually mask self-interest: evicting an indigobird egg may pose too much risk that the firefinch will damage her own eggs in the process.
Remarkably, it turns out that the unusual parenting behaviors of firefinches and indigobirds were responsible for the evolution of the current array of indigobird species, each associated with different hosts. Songs were the key. Each new indigobird species got its start when one or more females laid their eggs, accidentally or opportunistically, in the nests of a novel host. Their offspring, even in that first generation, comprised a new, reproductively isolated "song population" or "host race." When the offspring reached sexual maturity and began courtship, the males of the new song population sang the firefinch songs they had learned from their foster father. Female indigobirds chose the males that sang the songs the females had heard as chicks, songs imprinted in their memories. (As with most other songbirds, the male indigobirds sing, but the females do not.)
The result was that birds living in one area sorted themselves into mating groups according to the songs they sang and the kinds of finches that raised them. Once the mating groups formed, the stage was set for sympatric speciation. Genetic data show that the ten distinct indigobird species that now occur across Africa evolved not over millions of years, as is typical for other bird species, but over just tens of thousands of years. Such rapid emergence of distinct species is a remarkable example of both sympatric speciation and adaptive evolution.
Could we re-create and experimentally confirm the critical behavioral conditions that led to new indigobird species? To do so, we populated an aviary with a pair of village indigobirds (Vidua chalybeata), along with twelve pairs of Bengalese finches (Lonchura striata) and twelve pairs of red-billed firefinches (Lagonosticta senegala). The birds chose mates from among the available members of their own species, and began to breed.
As expected, the female indigobird in our aviary laid each of her eggs in the nest of a firefinch, her typical host, and then mated again. Typically she would lay one egg a day in a firefinch nest, then move on to another firefinch nest after one or two days of laying. We gingerly relocated some of the indigobird eggs we found in firefinch nests to the nests of Bengalese finches, a "novel" host.
Soon enough, the male indigobird chicks were imitating the songs of their new Bengalese finch parents. The crucial test came when the young indigobirds were ready to mate: we played a tape of indigobirds singing firefinch songs through one loudspeaker, and indigobirds singing Bengalese songs through a second loudspeaker. The female indigobirds raised by Bengalese parents clearly preferred the Bengalese songs, sexually approaching the speaker.
The same young indigobird mothers also laid their eggs in nests of the novel host, the Bengalese finch. The indigobirds made that choice even though nests of the host species their own mothers had intended to use--namely, the nests of the firefinch--were available in the same aviary. In a similar way, indigobirds in West Africa recently colonized two new host species, setting off the early stages of what could be more indigobird speciation.