When a 10-kilometer-wide hunk of burning space rock slammed into what is now the Gulf of Mexico 66 million years ago, it touched off widespread destruction, wiping out more than 75 percent of life on Earth. The Chicxulub asteroid, as it is called, is best known as the dinosaur killer. But although it doomed Tyrannosaurus rex and Triceratops, the sauropods and the hadrosaurs, the asteroid actually set one lineage of dinosaurs on a path to glory: that of modern birds.
Birds got their start more than 150 million years ago, evolving from meat-eating dinosaurs called theropods, and they attained an impressive degree of diversity in the first 85 million years or so of their existence. But the ancestors of today's birds—members of the neornithine lineage—were mere bit players compared with archaic birds such as the enantiornithines, which ruled the roost. When the asteroid struck, however, neornithine fortunes shifted. The impact extinguished all of the nonbird dinosaurs and most birds. Only the neornithines made it through that apocalyptic event. This clutch of survivors would give rise to one of the greatest evolutionary radiations of all time.
Today there are more than 10,000 bird species, making them the second most speciose class of vertebrate creatures alive, outnumbered only by the bony fish. They come in every shape and size—the land-bound ostrich tips the scales at more than 136 kilograms; the ever whirring bee hummingbird, less than two grams. They have colonized virtually every major body of land and water on the planet, from the sweltering tropics to the frozen poles. And they have diversified to fill a vast array of dietary niches, evolving adaptations to eating everything from microscopic algae to large mammals.
Incredibly, roughly half of these species are songbirds, which are characterized by a special voice box. The group includes the warblers, canaries, larks and other mellifluous singers but also the strident (to human ears, anyway) crows and their kin. To put that number in perspective, there are approximately as many living species of songbirds as there are of mammals.
How did this particular group of birds come to be so extraordinarily diverse? Biologists have long sought to answer this question, scouring the fossil record and DNA sequences of modern birds for clues. But apart from pinpointing where songbirds originated (Australia), many of these studies produced inconclusive or conflicting results. A detailed picture of where and when the lineages leading to modern songbirds split off from one another—and thus the factors driving this radiation—remained elusive.
In the absence of conclusive evidence to show how it all transpired, researchers have advanced a number of competing theories for songbird diversification that center variously on climate change, plate tectonics and sexual selection, in which mate preferences spur evolution.
Now a new finding has set the field atwitter. All songbirds, it seems, have a weird extra chromosome that does not appear to exist in other birds. The discovery suggests a genetic mechanism for creating barriers to reproduction between populations of a species, which promotes speciation. Much remains to be learned about this auxiliary package of DNA, but already some researchers are wondering whether it just might be the secret of the songbirds' dazzling evolutionary success.
Back Pocket Genes
The chromosome in question is called the germ-line-restricted chromosome (GRC), so named for its presence in reproductive cells—eggs, sperm and their precursors—but not the rest of the body's cells, called somatic cells. Progenitors of both eggs and sperm contain GRC, but by the time a sperm cell has developed fully, the GRC has been eliminated from it. The chromosome is thus transmitted to offspring via the mother exclusively.
Until recently the GRC was known only from two songbirds: the zebra finch and its close relative the Bengalese finch. It seemed to be an oddity of these two species, nothing more. But when researchers decided to look for it in other lineages of birds, a striking pattern emerged. In a paper published in the June 11 Proceedings of the National Academy of Sciences USA, Anna Torgasheva and Pavel Borodin of the Russian Academy of Sciences, Denis Larkin of the University of London and their colleagues report that all 16 of the songbird species they examined—a sample that included representatives from across the family tree of songbirds—had the GRC; none of the eight species representing other major bird groups did. What is more, the GRCs they found differed considerably from species to species—even between closely related ones—suggesting that the chromosome has evolved quickly in these different songbird lineages since it first appeared in their common ancestor an estimated 35 million years ago.
Cells of other organisms have previously been found to carry extra chromosomes called B chromosomes. But their occurrence is erratic, varying between members of the same species or even between different cells in the same individual. GRC, in contrast, is “an obligatory element in the germ line of song birds,” Larkin says. This ubiquity suggests that GRC is more influential than B chromosomes.
Exactly what GRC is influencing is largely a mystery, however—researchers know very little about what its genes actually do. But some hints have come to light. In another recent GRC study, which has been posted to the bioRxiv preprint server but not yet published in a peer-reviewed scientific journal, Cormac M. Kinsella and Alexander Suh of Uppsala University in Sweden and their colleagues found that the zebra finch GRC contains at least 115 genes, including some that have been shown to make proteins and RNA in the ovaries and testes of adult birds. This expression pattern hints that these genes may help guide the development of sperm and eggs. Other genes on the zebra finch GRC are comparable to genes that are known from mouse studies to be involved in early embryonic development.
To Borodin and Larkin, these findings suggest that the GRC may have allowed songbirds to circumvent key constraints on bird evolution. “The avian genome in general is very compact and conserved compared with, for example, the mammalian genome,” Larkin explains. The genomes of today's mammals range in size from less than two picograms to more than eight picograms and are packaged into anywhere from six chromosomes to 102. In the tens of millions of years over which they have been evolving, their chromosomes have been sliced and diced and reshuffled and rejoined many times. These rearrangements have altered gene expression in ways that have produced diverse traits. Birds, in contrast, have genomes ranging from just under one picogram to just over two. And they usually have right around 80 chromosomes, with comparatively little of the “junk” DNA found in most mammals.
The reason bird genomes are small and streamlined, some experts surmise, has to do with flight. Flying is an energetically expensive activity. Larger genomes require larger cells, and both are metabolically costlier than their smaller counterparts. The intense metabolic demands of flying may have therefore limited bird genome size. Because the GRC occurs only in germ-line cells and not the far more numerous somatic cells, it could have provided songbirds with a rare chunk of extra DNA—fodder for the evolution of new traits—without the metabolic costs associated with having a larger somatic genome.
“Birds need additional copies of germ-cell-specific genes for a very short breeding period only to produce a lot of sperm and load [egg cells] with large amounts of proteins. They have no reason to carry these genes throughout the year and in [the rest of the body's] cells when and where they are of no use,” Borodin says. If songbirds found a way to obtain additional genes on a temporary basis that could work during early stages of development while keeping their basic genome intact, Larkin adds, such an arrangement would be tremendously advantageous and could lead to the huge variety seen in songbirds compared with other bird groups.
In theory, the GRC could have created the reproductive isolation needed for new species to evolve by rendering those individuals that carried the extra chromosome unable to interbreed and produce fertile offspring with those that did not. Once the GRC originated in the last common ancestor of songbirds, members of that ancestral species that carried the GRC could produce fertile offspring only with mates that also had the GRC. As the GRC evolved, acquiring new genes, songbirds with a particular variant of GRC could produce fertile offspring only with mates that carried that same GRC variant.
Engine of Change?
According to Borodin and Larkin, the discovery that GRC is widespread among songbirds and absent in other birds dovetails with the results of another recent study. In April, Carl Oliveros of Louisiana State University and his colleagues reported on the results of their analysis of DNA from dozens of members of the passerine order of birds, which comprises the songbirds and some other, far less speciose groups. Based on the DNA sequences and a handful of fossils of known age, the team reconstructed how the various passerine families were related and when they branched off. It then compared this time line of diversification against climate and geologic records to see if the passerine diversification trends correlated with events in Earth history, as predicted by some hypotheses. On the whole, fluctuations in the diversification rates of these birds did not track changes in global temperature or dispersals of the birds into new continents. The findings prompted the authors to suggest that more complex mechanisms than temperature or ecological opportunity were the main drivers of passerine speciation. “These conclusions are very much in line with our hypothesis of GRC contribution to songbird diversification,” Larkin asserts.
Not everyone is ready to embrace the suggestion that GRC drove songbird diversification, however. “In general, it is hard to establish causation between any one given trait, like the presence of GRCs, and the evolutionary success of a particular group,” Oliveros says. “The presence of the trait could by chance have coincided with another trait—nesting behavior, for example—that may have played a larger role in a group's evolutionary success.”
But other researchers not involved in the new studies find the notion intriguing. “The fact that [GRCs] have been maintained over long evolutionary periods and also contain putatively functional genes ... suggests that they could play a role in reproductive isolation in birds,” observes David Toews of Pennsylvania State University. If the sky-high diversification rate of songbirds compared with that of other birds was promoted by a genomic mechanism such as GRCs, “it would definitely be exciting and not something that I would have predicted,” Toews says. He cautions, though, that “we need to know more about what they are actually doing to make that link with confidence.”
The work could have implications for understanding organisms beyond birds. “We thought we knew a lot about how bird genomes are organized,” Suh reflects, “but the GRC has been right before our eyes yet has been overlooked.” Scientists have found similar extra chromosomes in hagfishes and some insects. What if GRCs are more widespread in the tree of life, he wonders: “The findings in songbirds open up a bunch of new directions for thinking about evolution and development.”