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When Evolutionists Acquire Superhuman Powers: A Conversation with Peter and Rosemary Grant
David Sloan Wilson
David Sloan Wilson
is the SUNY Distinguished Professor of Biology and Anthropology at Binghamton University and Arne Næss Chair in Global Justice and the Environment at the University of Oslo

The modern evolutionist is like Darwin with superhuman powers of observation. Today it is possible to measure entire genomes and the patterns of gene expression (epigenetics); to trace neural pathways inside the brain; to track the movement of animals via satellite; to measure climate change in the distant past with a high degree of accuracy; to experiment with evolution in the laboratory using microbes that can be frozen and brought back to life to compare with their own descendants.

Remarkably, these technological advances do not make the basic theory of evolution old fashioned. On the contrary, Darwin’s achievement was to provide a theory that made sense of a vast body of information about plants and animals available during the 19th Century. The amount of information available to us might have increased by many orders of magnitude, but the same theory is performing its role of organizing the information remarkably well.

No one is in a better position to appreciate these points than Peter and Rosemary Grant, the celebrated couple from Princeton University who have been studying Darwin’s Finches on the Galapagos Islands for many decades, as chronicled for a general audience by Jonathan Weiner in The Beak of the Finch. When they started their research in the 1970’s, the tools of their trade were little different than during Darwin’s time: binoculars, field notebooks, a way to mark individuals, and hundreds upon hundreds of hours of painstaking observations. Over the decades, they have worked with dozens of colleagues to incorporate the latest techniques into their research on adaptation and speciation in the same natural laboratory that played such a formative role in Darwin’s thinking.

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David Sloan Wilson: Welcome, Peter and Rosemary, to This View of Life.

Peter Grant and Rosemary Grant: Thank you, we are glad to join you

DSW: Let’s begin at the beginning of your work in the Galápagos Islands. A landmark book on Darwin’s Finches had already been written (by the British evolutionary biologist David Lack in 1947) and you already had a career studying other species. What made you decide to focus on Darwin’s Finches? Did you know from the beginning that it would become your life’s work?

RG: Our overall goal was to understand more thoroughly the process of speciation, how and why species multiply. There were five reasons for choosing the rather drab Darwin’s Finches on the Galápagos as opposed to the more spectacular radiation of the Hawaiian Honeycreepers or Anolis lizards in the Caribbean. The radiation is young; we now know from molecular data that it is probably no more than 1-2 million years old. The full complement of species is present, none having become extinct as a result of human interference. The species occur together and separately on many islands uninhabited by humans that are close to pristine. Situated astride the equator the archipelago is subject to the El Niño-Southern Oscillation phenomenon bringing years of heavy rainfall interspersed with years of prolonged drought. Furthermore, as described by David Lack, many of these populations are highly variable in body size and bill dimensions. These five factors allowed the possibility of studying measurable changes over time under natural conditions.

PG: We had three specific questions in mind at the outset. First, was competition between species important in structuring the composition of groups of species that live in the same environment? It was an open question in 1973, with ecologists taking strong positions, affirmative or negative. Second, why do some populations vary so much in traits like body size or, in the case of birds, the size of their beaks, while other related populations of the same or different species vary much less? Third, the largest question of all, the Darwinian question–how do new species arise? We knew from David Lack’s Monograph, which each of us had read while undergraduates, that Darwin’s Finches could throw light on all three questions. But we never thought studying them would become a life’s work.

DSW: The scientific world is glad that it did! Is it accurate to say that the tools at your disposal were little different than during Darwin’s time? With the notable exception of computers for analyzing data!

PG & RG: Almost true, when viewed from 2016. But think of what we could do in 1973 that was out of Darwin’s reach, apart from marking birds so that we could establish their individual fates. We had a knowledge of genetics! Armed with that we could construct pedigrees and from these relationships estimate the genetic inheritance of traits like body size and beak size, and use inheritance to predict evolution when natural selection occurred. We had statistical tools to help us, and IBM computers to perform speedy calculations.

DSW: Right! I am guilty of hyperbole as charged. Also, I have learned from you that the technique of marking individuals in the field didn’t start until the end of the 19th century. What are some “superhuman powers of observation” that have become available over the years? Please provide as much detail as you like. TVOL readers enjoy a deep dive.

PG: Two developments helped us to peer into the genomes of finches. The first was the invention of tools to measure microsatellite DNA. With more than a dozen genetic loci we were able to characterize each finch with a unique DNA signature. The signature was invaluable for a range of studies that varied from determining paternity of individual finch offspring to comparing populations and species genetically. The second was the ever increasingly powerful methods of identifying genes. In the hands of our collaborators Cliff Tabin and Arkhat Abzhanov at Harvard the methods of functional genomics enabled them to identify Bmp4 and Calmodulin as important genes producing signaling molecules that influence the development of the depth and length of the beak respectively. In the hands of Leif Andersson and Sangeet Lamichhaney at Uppsala, whole genome sequencing enabled them to find two more genes, ALX1 and HMGA2, that code for transcription factors that affect beak shape and size.

RG: I would like to emphasize the power of these techniques for revealing evolutionary processes when combined with detailed fieldwork on individuals, because they enable us to identify the genetic underpinning of our findings on the changes that have occurred in populations through natural selection and introgression over time.

PG: A light-hearted footnote to our replies. One evening in 1978, while camping on the Galápagos island of Genovesa, we indulged in a fantasy worthy of scientific fiction. What if, one day, we could point an instrument like a telescope at a finch and get a complete readout of its genome transmitted by satellite to our computer in Princeton? Fantasy, may be, but its amazing how much closer we are to that vision with complete genome sequences now within reach. All we need now is someone to invent our genoscope!

DSW: Absolutely! Detailed fieldwork on individuals remains the essential core of your research program. Have these technological advances changed the fundamental questions that you ask?

PG: No, I would say the new technologies have helped us probe deeper into genomes to gain more detailed genetic answers to the original questions. Take character displacement as an example. Character displacement is a divergence of two competitor species caused by natural selection. Our field studies on Daphne Major Island showed that character displacement in beak size occurred when the large ground finch outcompeted large members of the medium ground finch for large seeds during the drought of 2004. The offspring of the surviving medium ground finches were, like their parents, relatively small, as expected from the beak inheritance. An obvious question is what were the genes involved in this evolutionary response to natural selection? The genomic study revealed one gene played a large role. It was HMGA2, a beak size factor. Although many genes were involved in the response, variation in this single gene accounted for nearly a third of the variation in survival. It was important to a disproportionate degree.

RG: A second example is the discovery of the ALX1 gene that encodes a transcription factor associated with beak shape. We had previously documented from our field observations on banded birds and an analysis of microsatellite data the rare but persistent incidence of gene flow between species through hybridization and subsequent backcrossing. After the El Niño event of 1983, when the island was converted from a large hard seed producer to a small seed producer, survival of Geospiza fortis x G. scandens hybrids increased. The beaks of hybrids are intermediate in beak shape, and are capable of dealing with small seeds efficiently. It turned out that the ALX1 gene comes in two forms in Darwin’s finches, a variant associated with blunt beaks (ALX1-B), and a variant associated with pointed beaks (ALX1-P). By going back into our -80C freezer we were able to retrieve the blood samples from fortis, scandens and hybrids of known measurements, and send the samples over to Sweden without telling our colleagues which ones came from birds with blunt beaks and which ones came from birds with pointed beaks. They were able to confirm two things. First, the two ALX1 haplotypes were associated with blunt and pointed beaks in the fortis population. Second, introgression of ALX1-P from scandens to fortis most probably increased the frequency of pointed beaks that were better adapted than blunt beaks to exploiting small seeds efficiently.

DSW: That’s an amazingly fine level of resolution! Can these techniques shed light on behavioral and life history traits, in addition to anatomical traits such as beak size?

PG: Yes, certainly, they are being used to understand such things as the evolution of resistance of mice to rodenticides, color vision in insects and fish, migration in birds and schooling behavior in sticklebacks.

RG: There are now increasing numbers of examples of hybridization with introgression. For example immune alleles passing from Neanderthals into modern humans most probably aided their adaptation to Northern Europe. Likewise high altitude adaptive traits were passed from Denisovans to Nepalese Sherpas.

DSW: What have the new techniques taught you about speciation—the great question that so many studies on adaptation and natural selection seem to dance around without directly addressing?

PG & RG: We will try to be brief. We have written two books on this topic; How and Why Species Multiply (2008) and 40 Years of Evolution (2014), both published by Princeton University Press. These discuss two types of discovery that inform us about the genetic mechanisms and ecological circumstances of speciation. First is the discovery of evolution in response to natural selection when the climatic environment changes: ecological adaptation. The second is hybridization followed by backcrossing. Almost by accident and without looking for it we stumbled upon introgressive hybridization as an ongoing and important process of evolutionary change. The lesson we learned from this is that an exchange of genes does not necessarily reverse the process of divergence and cause a collapse of two species into one. It can instead increase genetic variation in a recipient species and make it more likely to evolve along a novel trajectory. The new techniques have successfully revealed some of the genes involved in both adaptation and introgression. The emerging picture is a few genes have a major effect on a trait such as beak size and many other genes play minor roles. But the picture is far from complete. There are vastly more discoveries yet to be made, especially on the question of how different sets of genes are put together in workable combinations when species exchange genes.

BRG: In addition to the allopatric model of speciation, which we have supported with our own research, we have shown that introgressive hybridization in a new environment can lead to the formation of a new lineage; that is, incipient speciation.

DSW: Now let’s talk about the future. What are the biggest scientific questions that you and your colleagues are in a position to answer with Darwin’s finches as a model system?

PG: I regard the origin of biological diversity to be a major question for evolutionary biologists to address; some would say it is the major question. It is much more than speciation. It is a question of why the world is occupied by plants, animals and microbes, and how their distinguishing features arose. Answers will come from research by paleontologists, ecologists, behaviorists, geneticists, immunologists, virologists and other specialists. Within this broad framework the Darwin’s finch system can tell us about the small initial steps in the evolutionary divergence of populations; microevolution, in a word. It can tell us how fast evolution occurs, and what promotes it and what constrains it.

RG: And since the finches inhabit an entirely natural environment (on some islands) we can extrapolate without qualification from the causes and consequences of contemporary evolution to evolution in the past.

DSW: You have always worked with a network of colleagues and students but I imagine that this network has grown with all of these new technologies. How has that changed the character of your research? Is everything more of a group effort than it was before? Are there plans to insure that your legacy of studying Darwin’s Finches as a model system will continue?

PG & RG: Collaboration has changed the character of our research, from ecological, behavioral and quantitative genetic to genomic. We have been fortunate to have excellent collaborators (Cliff Tabin, Leif Andersson) who have done exciting research that we ourselves are not qualified to do: laboratory molecular genetic research. These have given us fast development along two new axes of discovery without altering the fundamental character of the field-based research. The latest collaboration with Leif Andersson’s group in Uppsala will continue in the foreseeable future. Our fieldwork ceased four years ago and we have no plans to resume, for several reasons. Other biologists are currently studying the ecology and evolution of Darwin’s finches on other islands.

DSW: This has been great fun. In closing, let me return to the main theme of this conversation: Evolutionary theory is needed to organize information about the living world, no matter the amount of this information. That’s why the theory never becomes old fashioned. If we increase the amount of information by many orders of magnitude, as we have with our superhuman powers of observation, then the need for an organizing theory becomes greater, not less. Thanks for helping me illustrate this point with your wonderful—and timeless–work on Darwin’s finches.

PG & RG: Well thank you! And do continue to write about the power and marvels of evolution, and reveal its hidden complexity!

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