Meet the Great Speciators: The White-Eyes

tags: evolution, speciation, diversification rate, Zosterops, White-eyes, ornithology, birds, molecular phylogeny, South Pacific Islands

For many decades, the white-eyes (Family: Zosteropidae) were known as the "Great Speciators" in honor of their apparent ability to rapidly give rise to new species while other birds in the same areas showed little or no diversification. But the Great Speciator hypothesis could only ever be indirectly inferred -- until now, that is. According to a paper that was just published by my postdoctoral colleagues, Rob Moyle and Chris Filardi, this group of diminutive birds apparently does evolve faster than any other avian group on earth.

This research -- the result of ten years in the field and five more years in the lab -- was a collaboration between my postdoctoral colleagues, Chris Filardi, a Biodiversity Scientist for the Pacific Programs at the Center for Biodiversity and Conservation at the American Museum of Natural History, and Rob Moyle, an Assistant Professor of Evolutionary Biology and Assistant Curator at the University of Kansas, Catherine Smith, a colleague of mine from graduate school, and the hypothesis co-developer, Jared Diamond, a Professor of Biogeography at the University of California at Los Angeles.

Together, my colleagues collected and studied the enigmatic White-eyes: a group of small olive-green passerines whose common name honors their most characteristic feature; the dramatic ring of tiny white feathers around their eyes, which gives the impression that they are wearing white-framed spectacles. Historically, the Zosteropidae dispersed across a large geographic area throughout the tropics and subtropics, from Asia to sub-Saharan Africa and Oceania, leaving numerous species along the way (Figure A);

The mechanism of this rapid radiation remained elusive for 80 years. Yet, so remarkable was the diversification of this lineage that the famous evolutionary biologist, Ernst Mayr, devoted a 1942 paper to exploring this phenomenon, and in 1976, biogeographer Jared Diamond coined the hypothesis name; "The Great Speciators." But how closely related are the white-eyes? How could they form so many distinct species -- often located very close together geographically -- when clearly, their dispersive way of life should aid gene flow and thereby prevent speciation? This conundrum is the Great Speciator Hypothesis's famous paradox.

To test this hypothesis and to gain an understanding of its famous paradox, the team sequenced nuclear and mitochondrial DNA isolated from individuals from 42 species of Zosteropidae and 23 species of the closely-related Timaliidae (Babblers). They analyzed those data to reconstruct evolutionary relationships among white-eyes, to assess their geographic and temporal patterns of diversification, and to determine diversification rates within the Z. [griseotinctus] species complex (Figure 1);

As you can see from the phylogenetic tree and the other accompanying data analyses, most of the 100-plus White-eye species evolved very recently and rapidly.

"As we started to compile the data, we were shocked," recalls Moyle. In short, the team found that "White-eye species from across the family's range had strikingly similar genetics, indicating a recent origin and incredibly rapid diversification."

Apparently, the Zosteropidae emerged as a group between 4.46 and 5.57 million years ago, and then radiated explosively into the roughly 80 named species within the genus Zosterops within just the last 2 million years. Based on these data, the team calculated the rate of diversification for Zosterops, and found that it is the fastest known rate of speciation for birds: between 2.24 and 3.16 species per million years.

"White-eyes evolved into dozens of new species extremely fast while simultaneously spreading across much of the hemisphere," Filardi told me last night in a late night phone call.

Only a few other vertebrates in the world are known to have a faster rate of speciation; most notably, the famous cichlid fishes found in lakes of the African Rift Valley, many of which are popular aquarium subjects in the United States. We now know that cichlid diversification occurred to meet the demands of climate shifts and geological changes within their narrow geographic range, while the rapid speciation among white eyes cannot be linked to environmental factors because of their recent hemispheric spread. Why is this particular lineage so adept at giving rise to new species?

"At this geographic scale," Filardi continued, "there is no one thing from the outside that could have made this happen; there is something special about those birds."

The team suggests that intrinsic life history traits of white-eyes actually drive speciation in this lineage. These traits include extreme sociability, the ability to survive in a variety of habitats, and a short time generation time when compared to other birds. Additionally, some species apparently have given up their dispersive lifestyle and "settled down," thereby minimizing gene flow so new species could form.

These data not only support the "Great Speciator" hypothesis but they also explain the famous paradox where some organisms can rapidly give rise new species while simultaneously dispersing over large geographic distances.

"This leaves the question: are the white eyes really special, or have we simply caught them at a special time in their evolution?" Filardi speculated. "That we don't know, but our results indicate that high rates of diversification may have as much to do with a species' 'personality' as they have to do with more classical geographic or geological drivers of speciation."

Using Skype, email, mobile phones and other modern technologies to send documents and data back and forth, Filardi went on to describe this work as a "true collaboration" where he and Moyle discussed and developed their data and ideas together.

"I am delighted to see this molecular evidence supporting ideas that I had only been able to guess at over the last several decades," remarked Diamond, who is very supportive of this collaboration. "I know that Ernst Mayr, if he had still been alive, would have been delighted at this confirmation 78 years after he visited the Solomons."

Sources

R. G. Moyle, C. E. Filardi, C. E. Smith, J. Diamond (2009). Explosive Pleistocene diversification and hemispheric expansion of a "great speciator." Proceedings of the National Academy of Sciences DOI: 10.1073/pnas.0809861105.

My friends and colleagues, Chris Filardi and Rob Moyle, who both are happy to answer your comments and questions in the comments thread.