The idea of ​​an Ice Age ‘cash pump’ in the Philippines spurred by a new way of drawing evolutionary trees

Is the amazing biodiversity of the Philippines partly the result of the rise and fall of the seas during the ice ages?

Scientists have long believed that the unique geography of the Philippines – coupled with jagged ocean levels – could have created a “species pump” that triggered massive diversification by isolating and then reconnecting again and again groups of species on the islands. They call the idea the “Pleistocene Aggregate Island Complex (PAIC) Model” of diversification.

But hard evidence, linking speciation bursts to specific times when global sea levels rose and fell, has been scarce so far.

A groundbreaking Bayesian method and new statistical analyzes of gecko genomic data in the Philippines show that during ice ages, the timing of gecko diversification gives strong statistical support for the PAIC, or “species pump” model for the first time. The investigation, with roots at the University of Kansas, was just published in the Proceedings of the National Academy of Sciences.

“The Philippines is an isolated archipelago, currently comprising more than 7,100 islands, but that number was greatly reduced, perhaps to six or seven giant islands, during the Pleistocene,” said co-author Rafe Brown, curator in charge. from the Herpetology Division of the Biodiversity Institute and the KU Museum of Natural History. “The aggregate landmasses were made up of many small islands today, which became joined together by dry land as sea levels fell, and all of this water was held in glaciers. One broadcast the hypothesis that this type of land fragmentation and melting, which has occurred as sea levels have fluctuated repeatedly over the past 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 that one does not found only in the Philippines.”

For decades, the Philippines has been a hotbed of fieldwork by biologists from KU’s Biodiversity Institute, where the authors analyzed genetic samples from Philippine geckos as well as other animals. However, even with today’s technology and the ability of scientists to characterize variation across the genome, the development of powerful statistical approaches capable of handling genome-scale data is still catching up. delay – especially in difficult cases, such as the task of estimating past times which species formed, using genetic data collected from populations surviving today.

Lead author Jamie Oaks of Auburn University and co-author Cameron Siler of the University of Oklahoma were both KU graduate students advised by Brown. They were joined by co-author Perry Wood Jr., now at the University of Michigan, who recently worked at Auburn with Oaks and, earlier at KU with Brown, as a postdoctoral researcher.

For two centuries, naturalists who have studied species distribution in the Philippines have discussed, debated, and written extensively about the ideas behind the modern species pump theory or, in the Philippines, the predictions that now make up the “PAIC paradigm”. Historically, researchers focusing on particular animals or plants have endorsed the general idea, but others have expressed skepticism because it didn’t seem to hold up in other species they were studying.

“Over the last quarter century, with the widespread availability of genetic data, the specific predictions of the model have been much more rigorously, objectively and quantitatively tested – with real data from natural populations – which has been a breakthrough. major in Philippine biogeography,” Brown said. said. “In some animals and plants, the predictions held. But in others, when the same predictions were tested with real data and sufficiently rigorous statistical methods, they were repeatedly rejected. In many of our own studies at KU, when we looked at corollaries of the PAIC model in individual genera or groups of closely related species, we were surprised to find that the time window of ice ages was not even related to a large part of the diversity of species that we find today of bats, or a group of frogs, we found that fewer and fewer of today’s species seemed to have diverged in the Pleistocene. , with an accumulating lack of evidence, we kind of rephrased the question. We went back to the data from all these previous studies and asked – across all these dif different groups of animals, can we find statistical support for the formation of species, grouped in the Pleistocene time window? And the answer kept coming back ‘no’ – until now.”

Brown said the key to understanding the genomic evidence came from Oaks, who began examining gecko groups with a new approach to designing phylogenetic trees. Instead of one species branching off from another in isolation – as phylogenetic trees are traditionally drawn – a plethora of new species could branch off at about the same time into something that looks more like a “shrub” than to a tree.

“Shared ancestry underlies everything in biology, whether it’s a gene sequence, a viral strain, or a species,” Oaks said. “Each branching point on a phylogenetic tree represents biological diversification – for example, one species diverging into two. We have long assumed that 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, environmental changes will affect entire communities of species, not just one. Our approach allows multiple species to diversify through a shared process. In doing so, we are now better equipped to ask questions about these processes and test the patterns they predict.”

By relaxing the assumption of independent divergences, genomic data from Philippine geckos supported patterns of shared divergences, as “predicted by the repeated fragmentation of the archipelago by interglacial sea-level rises,” according to the researchers.

“This kind of shared divergence pattern 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 were widespread across the Philippines long before the start of glacial cycles, and so we know they were present on the larger islands. from the Ice Age, when they were fragmented by sea-level rise. We used information from their genomes to reconstruct their phylogenetic trees and test patterns of shared divergence predicted by the island fragmentation hypothesis We found support for these models, and now we see evidence of the effect of glacial cycles, but it’s important to remember that the overall phylogenetic history of these lizards is consistent with a more complex story.”

With this part of the “species pump” hypothesis now supported in the Philippines, Brown said there are many more cases where biogeographers could use the same approach to detect geographic or environmental changes that triggered explosions. biodiversity similar.

“The idea that a barrier could affect unrelated groups like birds, frogs, lizards and insects – perhaps impacting entire faunas at the same time – is something evolutionary biologists have long grasped. But strong support for the simultaneity of the timing of these processes has been a bit elusive,” Brown said. “There are many theories about shared mechanisms, and the ‘species pump’ idea is just one. between them. But, in general, common mechanisms of diversification, or shared processes of speciation, have always been important and exciting topics for evolutionary biologists, especially biogeographers.”

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