Does the astounding biodiversity of the Philippines have anything to do with the ice ages’ rising and declining sea levels?
Long believed by scientists to have caused a “species pump” that caused huge diversity by repeatedly isolating and rejoining groups of species on islands, the Philippines’ distinctive geology, and fluctuating ocean levels. The concept of diversification is known as the “Pleistocene Aggregate Island Complex (PAIC) model.”
But up until now, there hasn’t been any concrete evidence linking speciation booms to the particular dates that sea levels increased and fell around the world.
The timing of gecko diversification during the ice ages provides substantial statistical support for the PAIC model, or “species pump,” for the first time, according to a ground-breaking Bayesian approach and new statistical analyses of genomic data from geckos in the Philippines. The study, which had its origins at the University of Kansas, was just released in the Proceedings of the National Academy of Sciences.
“The Philippines is an isolated archipelago, currently including more than 7,100 islands, but this number was dramatically reduced, possibly to as few as six or seven giant islands, during the Pleistocene,” said co-author Rafe Brown, curator-in-charge of the herpetology division of the Biodiversity Institute and Natural History Museum at KU.
“The aggregate landmasses were composed of many of today’s smaller islands, which became connected together by dry land as sea levels fell, and all that water was tied up in glaciers. It’s been hypothesized that this kind of fragmentation and fusion of land, which happened as sea levels repeatedly fluctuated over the last 4 million years, sets the stage for a special evolutionary process, which may have triggered simultaneous clusters or bursts of speciation in unrelated organisms present at the time. In this case, we tested this prediction in two different genera of lizards, each with species found only in the Philippines.”
The scientists examined DNA samples of Philippine geckos as well as other animals in the Philippines, where biologists at KU’s Biodiversity Institute have been conducting fieldwork for decades.
Even with today’s technology and the ability of scientists to characterize variation across the genome, however, the development of strong statistical approaches capable of handling genome-scale data is still catching up. This is especially true in difficult cases, like the task of estimating the past times that species formed using genetic data collected from populations that are still alive today.
The idea that some barrier could affect unrelated groups like birds, frogs, lizards, and insects possibly impacting whole faunas together at the same time has been something evolutionary biologists have been grasping at for a long time. But strong support for simultaneous timing of these processes has been kind of elusive. There are lots of theories about shared mechanisms, and the ‘species pump’ idea is just one of them. But, in general, common mechanisms of diversification, or shared processes of speciation, have always been big, tantalizing topics for evolutionary biologists, especially for biogeographers.
Rafe Brown
Cameron Siler, a co-author from the University of Oklahoma, and Jamie Oaks, the lead author from Auburn University, were both graduate students at KU that Brown advised. They were joined by co-author Perry Wood Jr., now at the University of Michigan, who had previously worked as a postdoctoral researcher with Oaks and Brown at KU and Auburn.
The concepts behind the contemporary species pump theory, or, in the Philippines, the predictions that currently make up the “PAIC Paradigm,” have been extensively discussed, contested, and written about by naturalists who researched species distributions in the Philippines for two centuries.
The overall hypothesis has historically been supported by researchers specializing in particular animals or plants, but others have expressed skepticism because it didn’t seem to hold true in other species they researched.
“Over the last quarter century, with widespread availability of genetic data, the model’s specific predictions have been tested much more rigorously, objectively, and quantitatively with real data from natural populations which was a major step forward in Philippine biogeography,” Brown said.
“In some animals and plants, predictions held up. But in others, when the same predictions were tested with real data and appropriately rigorous statistical methods, they were rejected over and over. In many of our own studies at KU, when we examined corollaries of the PAIC model in individual genera, or groups of closely related species, we were surprised to find the ice ages time window wasn’t even related to much of the species diversity we find today. In study after study, individually focusing on a genus of bats, or a group of frogs, we found that fewer and fewer of today’s species seemed to have diverged in the Pleistocene. At that point, with a lack of evidence piling up, we kind of rephrased the question. We went back to the data from all those earlier studies and asked across all these different groups of animals, can we find any statistical support for species formation, clustered in the Pleistocene time window? And the answer kept coming back ‘no’ until now.”
Brown claimed that Oaks, who began examining gecko groups with a novel method for constructing phylogenetic trees, provided the key to comprehending the genomic findings.
A multitude of new species may branch away at nearly the same time in something that resembles a “shrub” rather than a tree, as opposed to one species branching from another in isolation as phylogenetic trees are normally represented.
“Shared ancestry underlies everything in biology, whether it’s a gene sequence, viral strain, or species,” Oaks said. “Each branching point on a phylogenetic tree represents biological diversification for example, one species diverging into two. We have long assumed the processes responsible for these divergence events affect each species on the tree of life in isolation. However, we have long appreciated that this assumption is likely often violated. For example, changes to the environment will affect whole communities of species, not just one. Our approach allows multiple species to diversify due to a shared process. By doing so, we are now better equipped to ask questions about such processes and test for the patterns they predict.”
The genomic data from Philippine geckos corroborated common divergence patterns by modifying the premise of independent divergence, as “predicted by repeated fragmentation of the archipelago by interglacial rises in sea level,” according to the researchers.
“This type of pattern of shared divergences can now be tested with our new phylogenetic approach,” Oaks said. “Gekko and Cyrtodactylus are two genera of geckos that are good test cases to look for these patterns, because they have been widespread across the Philippines since long before glacial cycles started, and so we know they were present on the large ice age islands when they were fragmented by rising sea levels. We used information from their genomes to reconstruct their phylogenetic trees and test for patterns of shared divergences predicted by the island-fragmentation hypothesis. We did find support for such patterns, and now we see evidence for the effect of the glacial cycles, but it’s important to remember that the overall phylogenetic history of these lizards is consistent with a more complex story.”
Brown said that there are numerous additional instances where biogeographers may apply the same method to identify spatial or environmental changes that sparked similar bursts of biodiversity. This portion of the “species pump” hypothesis has recently been validated in the Philippines.
“The idea that some barrier could affect unrelated groups like birds, frogs, lizards, and insects possibly impacting whole faunas together at the same time has been something evolutionary biologists have been grasping at for a long time. But strong support for simultaneous timing of these processes has been kind of elusive,” Brown said.
“There are lots of theories about shared mechanisms, and the ‘species pump’ idea is just one of them. But, in general, common mechanisms of diversification, or shared processes of speciation, have always been big, tantalizing topics for evolutionary biologists, especially for biogeographers.”
