How One Becomes Two: Genetic Shuffling Gave Rise To A New Bird Species
Sudden changes in bird songs and plumage colors provides female songbirds with mate choices that can rapidly lead to establishment of new species in closely related birds — a finding that challenges the typical model of how new species form
Speciation — the process underlying how one species becomes two — is a poorly understood but critically important evolutionary process that creates and defines all living things. My enduring passion to understand this seemingly straightforward mechanism is certainly what lured me into a career in science. But as if comprehending this mysterious process isn’t challenging enough, understanding how new species arise when they live beside each other and share the same habitat — and even eat the same things — is even more confounding.
Established species are typically separated by post-mating barriers to reproduction, such as genetic incompatibilities, which often take a long time to develop between closely-related animal species. But incipient species are often separated by pre-mating isolation, which typically are differences in ecology or behavior that influence their mate choices and prevent them from interbreeding. So studying wild populations of closely related that live alongside each other can shed light on our murky knowledge for how reproductive isolation can drive and nourish rapid speciation.
The same but different
This is where a remarkable group of songbirds is helping us. The southern capuchino seedeaters (genus: Sporophila) is a group of at least ten songbird species that radiated very rapidly within the past million years despite living and breeding in the same geographic location. (In contrast, the evolutionary split between humans and chimpanzees is estimated to have occurred somewhere between five and six million years ago.) The southern capuchino seedeaters are one of the most rapid avian radiations on the planet and consequently, these bird species have almost imperceptible differences in both their ecology and genomes.
Despite their genetic uniformity, a 2017 study did uncover a few tiny genomic regions that are involved the regulation of plumage color and patterning for different capuchino seedeater species (more here). Although they are small, these genomic differences have enormous effects: Adult males of different species have dramatically different plumage colors and patterns whilst adult females and juveniles are visually indistinguishable. In addition to their striking genomic similarities, this group of birds also has remarkably low levels of ecological divergence; living alongside each other in the same area, and eating the same foods.
Seven of the ten (or so) known capuchino seedeater species breed within the vast swampy grasslands of the Iberá National Park, a newly created national park in northeastern Argentina. These finch-like songbirds are smaller than a canary and have short, stout bills that are adapted for opening seeds. Most capuchino seedeater species are strongly sexually dimorphic; with males showing dramatically different plumage colors and patterns from females and juveniles, which all appear identical to human eyes, regardless of species (figure 1, right panel).
“The capuchino seedeaters of South America are what we call a ‘species flock’,” the senior author of the study, evolutionary biologist Leonardo Campagna, a research associate at the Cornell Lab of Ornithology, said in a statement. “This group is branching out rapidly and each of its dozen species is in a very early stage of evolution.”
When a new species of seedeater, the Iberá seedeater, Sporophila iberaensis, was first observed in 2001, and scientifically described in 2016, it was noted that this species breeds side-by-side with its very close relative, the tawny-bellied seedeater, Sporophila hypoxantha. Although it is increasing in local abundance, the Iberá seedeater has a very small and restricted breeding range whereas the tawny-bellied seedeater is the most abundant and widespread capuchino species in Iberá National Park.
Adult males of these two species are easy to distinguish at a glance: Adult male Iberá seedeaters have black cheeks and throat, pale grey underparts, darker grey wings and back (figure 1, left panel). In contrast, adult male tawny-bellied seedeaters have rust-colored cheeks, throat and underparts with dark grey wings and back (figure 1, center panel). Both species have dark eyes, bills, legs and tails. How did the Iberá seedeater appear so quickly and how does it remain distinct from its closest relative, the tawny-bellied seedeater?
Genetic shuffling may be the engine of speedy speciation
“We compared the most recently discovered species, the Iberá Seedeater, with what is likely its closest relative, the Tawny-bellied Seedeater,” Dr Campagna explained. “Because they’re so alike genetically, it’s easier to find where their genomes differ and what traits arose from those genetic differences. The bottom line is, how did this new Iberá Seedeater come to be?”
To answer this question, the study’s lead author, Sheela Turbek, a behavioral ecologist and PhD Candidate at the University of Colorado Boulder, and her collaborators pursued this rare opportunity by comparing the complete genomes of the two species. Remarkably, they uncovered genetic differences in just three small regions located on different chromosomes. These regions contain a total of just 12 genes, 3 of which are involved in plumage coloration.
“We found that the Iberá Seedeater likely formed through past hybridization between capuchino species and the subsequent reshuffling of genetic variation into novel combinations encoding differences in male plumage patterning,” Ms Turbek explained in email. “This result suggests that access to old genetic variants that can be recombined to form novel mating signals may be a major factor explaining why capuchino seedeaters were able to diversify so rapidly.”
Surprisingly, this novel mixing and matching of existing genetic traits already found in closely related species can create something new — and it creates it very quickly.
“These differing genes have been reshuffled into a unique combination that produced the Iberá Seedeater,” Dr Campagna elaborated. “This species has a mosaic of plumage genes drawn from existing genetic variation already found in other seedeater species. As a rough estimate, it took perhaps a few thousand generations for the lineage with this new plumage variation to evolve into a separate species that would only mate with its own kind. In evolutionary terms, that’s very fast!”
Observing these birds as they breed side-by-side provides a valuable opportunity to study these species’ mate choices and other reproductive behaviors. Previous field studies suggest that divergent male traits, particularly song, strongly impact conspecific recognition and territorial defense (ref). And yet, capuchino seedeaters can produce viable hybrids both in the field (ref) and in captivity (ref), demonstrating that they lack species-specific genetic incompatibilities.
Choosy females drive rapid speciation in birds that share a home
But how do the birds themselves perceive their plumage colors and songs? To better understand which traits are involved in species recognition, Ms Turbek conducted a series of behavioral field experiments on males with established territories. She painted bird decoys with the colors and patterns of male Iberá and tawny-bellied seedeaters, set them up in a study male’s territory, played recordings of the species songs and watched the reactions of the resident birds. Basically, ‘bird hell’ broke loose.
“Color and song are important because they allow species to recognize each other,” Ms Turbek pointed out in email. “So they become isolated from a reproductive point of view, despite breeding side-by-side with the other species.”
These field studies demonstrated that territory-holding males of the two seedeater species specifically recognize males that look like them and sing like them, and react react most aggressively towards them (see video & figure 3).
“We exposed territorial males of both species to their own color and song, then switched up the colors, and switched up the song, in all of the possible combinations,” Ms Turbek explained. “Each species responded most aggressively to models that looked and sounded like themselves, apparently considering them sexual rivals.”
“We found that males of both species responded more aggressively to their own song and plumage than those of the other capuchino species, suggesting that both traits are jointly used to identify members of their own species as sexual competitors, and by extension, may be involved in female choice.”
But since females are ultimately choosing their mates, they are the ones whom the males must impress. Which is more important trait to the females: plumage color or song? Unfortunately, due to the remoteness of the location and the endangered status of the Iberá seedeater, this experiment is logistically impractical.
“However, our behavioral experiment attempted to indirectly address this question by presenting males of the Iberá Seedeater and Tawny-bellied Seedeater with various combinations of plumage and song and recording their aggressive responses,” Ms Turbek replied in email.
Because female capuchino seedeaters are visually indistinguishable to human eyes, Ms Turbek and her collaborators used genomic data to quantify assortative mating. Most people are unfamiliar with this term, but we are often acutely aware of it in practice. Assortative mating is the tendency to choose mates whose observable (phenotypic) traits are more or less similar than would be expected by chance — these include physical or cultural traits such as religion, nationality, height, or age, just to name a few.
In capuchino seedeaters, the traits they use to choose a mate are plumage color and pattern, and song. Basically, females select their mates based on (1) their genetically inherited plumage color and (2) their culturally inherited song types, and thus, assortative female mate choice is the primary mechanism promoting and maintaining early and rapid divergence between these two seedeater species that breed in the same place, nest at the same time, eat the same foods, and are almost genetically identical.
“Each female’s species-specific genotype always matched the genotype of her mate, demonstrating strong assortative mating despite these two species holding neighboring breeding territories, breeding synchronously, and foraging together on the same grasses,” the authors wrote in their study (ref).
“Capuchino seedeaters are one of the clearest examples showing how existing genetic variation may be reshuffled into novel combinations to generate novel signaling traits involved in mate choice,” Ms Turbek said in email. “This mechanism of speciation can occur quite rapidly because it doesn’t rely on the long period of time usually required for novel mutations to arise that limit interbreeding between closely related organisms.”
This same genetic shuffling process probably governs the origin of the other 12 capuchino seedeater species, each of which arose recently from a common ancestor. Such novel recombinations of existing traits probably occur when a hybrid is born. A hybrid is a natural experiment that could easily have generated the many different seedeater species through a recombination of a variety of black, yellow, red or white throats, paired with differently colored caps, underparts, and other key identifying features.
But this genetic mechanism is not unique to capuchino seedeaters.
“[A] similar mechanism of speciation has been implicated in the recent radiation of Lake Victoria cichlids, which have diversified over the past 200,000 years to form a spectacular array of species characterized by differences in male coloration,” Ms Turbek pointed out in email.
In fact, many rapid radiations of new lineages may arise from mix-and-match hybrid events rather than from multiple genetic mutations accumulated in geographic isolation over millions of years. These rapid speciation events include Darwin’s finches (more here), Heliconus butterflies (more here), and Hawaiian silverswords probably arose from new combinations of genetic variants that existed prior to the diversification of these groups. As more and more studies examine radiations using whole-genome sequencing, we may discover that this mechanism of speciation is fairly common.
Further, examining the females’ mating choices reveal they are a powerful force for promoting and maintaining early and rapid divergence between these two seedeater species.
“We also demonstrate that differences in song and plumage alone may be sufficient to maintain species boundaries extremely early in divergence and allow the accumulation of additional barriers that prevent interbreeding between co-occurring taxa.”
“Understanding what drives the variation in speciation rates that we observe across the tree of life is a major goal of evolutionary biology,” Ms Turbek said in email.
“Our study indicates that new organisms can form and quickly become isolated from co-occurring species through the reshuffling of existing genetic variation into novel combinations that encode traits used in mate choice. This mechanism of speciation can occur quite rapidly because it doesn’t rely on the long period of time usually required for novel mutations to arise that limit interbreeding between closely related organisms.”
Sheela P. Turbek, Melanie Browne, Adrián S. Di Giacomo, Cecilia Kopuchian, Wesley M. Hochachka, Cecilia Estalles, Darío A. Lijtmaer, Pablo L. Tubaro, Luís Fábio Silveira, Irby J. Lovette, Rebecca J. Safran, Scott A. Taylor, and Leonardo Campagna (2021). Rapid speciation via the evolution of pre-mating isolation in the Iberá Seedeater, Science, 371(6536):eabc0256 | doi:10.1126/science.abc0256
Originally published at Forbes.com on 31 March 2021.