In a 2006 paper in Science, Peter and Rosemary Grant provided evidence that demonstrated a character displacement event in a Galapagos finch species. This was, probably, the first such documentation of character displacement in the wild. Ten years after the paper was published, I spoke to Peter and Rosemary Grant about the making of this study, and how this work has progressed since then.
(Interview conducted over email between 9th September 2016 and 30th November 2016)
Citation: Grant, P. R., & Grant, B. R. (2006). Evolution of character displacement in Darwin's finches. Science, 313(5784), 224-226.
Hari Sridhar: The motivation for this paper was the character displacement event you observed in Geospiza fortis in 2004-2005, what you call "the strongest evolutionary change seen in the 33 years of the study". What has happened in the next 10 years (2006-2016), in this character displacement story? If you were to extend the x-axis of Figures 2 and 3 to 2016, what would they look like?
Peter Grant & Rosemary Grant: No change from 2005 to the end of the study in 2012: a straight horizontal line on the graph of time.
HS: Is "no change" the case for the population graph (Fig. 3) as well? Does this continue to be the "strongest evolutionary change" you have detected so far in this system?
PG & RG: Regarding Fig. 3, numbers of both species rebounded after the drought, fortis more than magnirostris. Because there was no further change in the fortis trajectory, there was no more strong selection; so the 2004-06 episode of selection plus evolution remained the strongest in 40 years. Incidentally, if you have access to our most recent book you will see the full 40 years of morphological data (P. R. Grant & B. R. Grant 2014. 40 Years of Evolution. Darwin's Finches on Daphne Major Island. Princeton University Press, Princeton, NJ). 2012 was the last year of the field study.
HS: What was the spark that ignited the idea for this work and this paper? Were you looking out for it right from the time G. magnirostris established a breeding population on Daphne in 1982? Or was it initiated by the dramatic character displacement observed in 2004?
PG & RG: To answer this question, we have to go back to the early 1970s for the origin of interest in this subject. At that time, I (PG) reviewed the evidence for ecological character displacement and found it to be generally weak. Certainly, patterns of variation in nature could be interpreted as the product of competitive interactions between species, but the problem was that each of the patterns could be explained in alternative, non-competitive ways. One of the motivations of our initial work in the Galápagos was the desire to do better. In his 1947 monograph on Darwin’s Finches, David Lack had pointed out some apparently clear-cut patterns. For example, on the small island of Daphne Major, the medium ground finch (Geospiza fortis) was smaller than elsewhere, and because the small ground finch (G. fuliginosa) was absent from the island, Lack argued that the medium ground finch had taken over the niche of the missing species. On other, larger, islands both species were present and morphologically very distinct. Since Daphne had probably been colonized from nearby, larger and older Santa Cruz, this seemed like an example of the opposite side of the character displacement coin - character release as it has been called. Thus, part of the research we began in 1973 was designed to test the hypothesis of character or competitive release. Then, about a decade later, Daphne was colonized by the large ground finch (G. magnirostris). When it became clear this was not an ephemeral event, and that large ground finches were more efficient at exploiting the large and hard seeds of Tribulus cistoides than the large members of the medium ground finch population, we started to wonder if, one day, large ground finches could have a competitive influence on medium ground finches. This did indeed happen, twenty-two years after the initial colonization.
HS: Please tell us a little about the actual writing of this paper. At what point in the process did you start writing the paper and when and where did you do most of the writing? Did this paper have a relatively smooth ride through peer-review and was Science the first journal you submitted this to?
PG & RG: It did not take us long to convert the data into a paper, because the results of all analyses were clear and interpretable. We started analysing and writing when staying with our daughter and family in Corvallis, Oregon, and finished it in Princeton. We held back from publishing until we had been able to return to the field in 2006 to check whether the next generation of fortis remained, like their parents, displaced morphologically (see Fig. 2) from the pre-drought position. They had. So we finished the paper and submitted it to Nature. The editor rejected it without review because of “insufficient interest to researchers in a broad range of other disciplines”. Therefore we promptly reformatted the manuscript and submitted it to Science. Here it had a completely different reception. The manuscript was sent out for review, and all three reviewers plus editor were highly enthusiastic about it. The paper was accepted with some minor changes at the end of May and published six weeks later. Almost exactly 10 years later Science published our follow-up paper, where we provided a genomic understanding of what happened during the character displacement episode. But that is another story, and we will be happy to share it if you wish.
HS: Yes, please do tell us more about the follow-up genomics work, and if it was also followed up in any other ways.
PG & RG: We continued the fieldwork for seven more years after the character displacement event, to determine the long-term outcome of introgressive hybridization, and to follow the fate of the new lineage we had discovered. We will be glad to discuss this later. 2012 was the last year of fieldwork. Even before then we had started to synthesize the long-term research in order to write a book about the Daphne study. The book was published in 2014 by Princeton University Press (40 Years of Evolution. Darwin’s Finches on Daphne Major Island).
The genomic work began with a small problem of trying to understand the genetic basis of a beak colour polymorphism in finch nestlings. Beaks are yellow or pink. In 2010, we discovered a paper had been written about the same kind of colour polymorphism in chickens. It was by Leif Andersson’s group at Uppsala. We were put in touch with Leif by a mutual friend - Phil Hedrick at Arizona State University. That was the start of our collaboration. We found strong evidence of a simple mutation that accounted for the polymorphism in most populations of finches. One thing led to another, and we shifted the focus to the larger questions of finch genome variation and evolution. This work has led to two major papers so far. First, we published a paper in Nature that used genomic data to reconstruct the phylogeny. We also reported discovery of a gene, ALX1, which is a transcription factor affecting the development of beak shape. A mutation in the same gene in humans gives rise to cleft palate. Second, we published a paper in Science this year on the genomic follow-up to the character displacement paper a decade earlier. In the new paper, we reported the discovery of another gene influencing beak development through transcriptional activity. This is HMGA2, and it comes in two forms in finches. One is present in species with large beaks and the other is present in species with small beaks. These two variants are correlated with beak size among members of the Daphne population of fortis, with heterozygotes being intermediate in average beak size as expected. We found that genotypes associated with large beak size were at a strong selective disadvantage in the drought of 2003-04. The selection coefficient, 0.59, is exceptionally strong for natural selection on a continuously varying trait in a natural population. In fact, variation in haplotypes statistically explained approximately one third of the variation in the shift in average beak size. So, although many genes govern beak size, as we know from heritability estimates, we had discovered a single gene with a major effect on beak size, and it played a large role in character displacement. Interestingly, beak shape did not change during the character displacement episode, nor did the frequency of ALX1 haplotypes.
HS: Please tell us a little more about the work you did to determine the outcome of introgressive hybridization and the fate of the new lineage.
PG & RG: At the beginning of 2005, fortis were smaller on average than at any time in the preceding 32 years, and the question was whether they would stay that way or gradually change back to their pre-drought size, as happened after the drought of 1977. Offspring of the survivors of the 2004 drought were, on average, almost the same size as their parents, as we expected from the very high heritability of body size and beak dimensions. And in fact, average body size and beak size remained small right up to the end of our field study in 2012. Therefore, character displacement was not ephemeral: it persisted for seven years.
Part of the reason for a lack of change after 2005 is introgressive hybridization. G. fortis receives genes from fuliginosa, a smaller species, and scandens, a larger species. Genetic inputs from these two sources appear to have been roughly equal and hence contributed to the maintenance of the status quo.
Another part of the reason for lack of change is the flourishing of the Big Bird lineage after the character displacement event. We should first explain what the lineage is and how it formed. The lineage was initiated by a particularly large finch (hence the name Big Bird) that arrived on Daphne Major Island in 1981. Microsatellite DNA data suggested it was a fortis x scandens hybrid that had immigrated from nearby Santa Cruz Island. It bred with fortis, and two generations were produced before the drought of 2003-04. Two members of the lineage, a brother and a sister, survived the drought and bred with each other in 2005, as well as in the following years. Remarkably, their offspring bred with each other or with their parents, so did the grand-offspring. In breeding entirely endogamously the lineage behaved like a new species.
Big Birds occupy the morphological gap between magnirostris and fortis. The gap widened as a result of character displacement in fortis, and thus the Big Birds were less constrained by potential competition for large seeds from large members of the fortis population. The Big Birds have flourished because their diet in the dry season is varied, encompassing the large seeds eaten by magnirostris, the small seeds eaten by fortis, and nectar, pollen and seeds of Opuntia cactus eaten by both of them as well as by scandens, the cactus finch. The Big Birds are thus a central generalist in the Daphne community of finches.
We have recently taken the eco-morphological study into the realm of genomics by collaborating with Leif Andersson and his molecular genetics group in Uppsala, Sweden. The goal has been to investigate character displacement as a genetic phenomenon. The group discovered two genes that influence the development of beak traits through transcription factors. One of them, ALX1, affects beak shape. The other, HMGA2, affects beak size. Each gene comes in two forms: two haplotypes. In the character displacement event, the haplotype of HMGA2 that is associated with large beaks was at a strong selective disadvantage and declined in frequency. This demonstrates at genetic level what we had previously shown at phenotypic level. Interestingly fortis receives ALX1 and HMGA2 haplotypes from both fuliginosa and scandens. The HMGA2 haplotype from fuliginosa appears to have enhanced the evolutionary response in 2005 to natural selection in 2004.
To conclude, the community of finches on Daphne Major Island has changed from a 2-species community to a 4-species community. The character displacement episode played a pivotal role in the ecological adjustment of one species to another. It was caused by one of the additional species (magnirostris) and apparently facilitated the expansion of the other addition (Big Birds). The frequency of an important gene affecting beak size underwent a strong change. Introgressive hybridization with fuliginosa and scandens contributed to the evolution of fortis. We are currently using genomics to gain a deeper understanding of the consequences of introgression and the success of the Big Bird lineage.
HS: How was the paper received, both within academia and in the popular press, when it was published? Did it attract a lot of attention?
PG & RG: The paper was received very favourably in the scientific literature, and that has continued in both scientific papers and in books. We cannot recall any attention given to it in the popular press.
HS: In concluding your paper, you say "Replicated experiments with suitable organisms are needed to demonstrate definitively the causal role of competition, not only as an ingredient of natural selection of resource-exploiting traits but as a factor in their evolution. Our findings should prove useful in designing realistic experiments, by identifying ecological context (high densities at the start of an environmental stress) and by estimating the magnitude of natural selection." Today, 10 years after this paper was published, could you reflect on whether and to what extent this has happened?
PG & RG: The adjustment species make when brought into competitive conflict is still studied mainly opportunistically and observationally, not experimentally, by researchers alert to the possibility of character displacement. Three years ago, Yoel Stuart and Jonathan Losos reviewed more than one hundred reported cases of ecological character displacement. By applying strict criteria to the evidence, they concluded that only six cases (including Darwin’s finches) passed their test. Given so few examples documented in nature, it should be no surprise that experimental tests of the role of competition in character displacement in nature have not been done. The closest to our proposal was a study of sticklebacks in the laboratory by Dolph Schluter (1994). Microcosms have been investigated experimentally in the laboratory where conditions are strictly controlled and feasible mechanisms demonstrated. However, they do not address the question of applicability to processes in nature, or whether the results can be scaled up from micro- to macro-organisms and environments. Perhaps the best system for research in the field would be annual plants that have recently come into contact and shown evidence of competitive interaction. A promising environment might be alpine or subalpine habitat, where species ranges are shifting under climate change and previously separated species are now encountering each other.
HS: Today, in retrospect, is there anything that you wish you had done differently, or any other data you wish you had collected, at the time of the character displacement event in 2006?
PG & RG: It would have helped if we had quantified the seed supply before, during, and after the character displacement event by random sampling, just as we had done in every year from 1976 to 1991. However, given our observations, on the difficulty finches experienced in finding Tribulus fruits during the 2003-04 drought, we are quite confident that sampling data would have revealed a very strong decline in availability.
HS: In the paper, you acknowledge "K.T. Grant, L.F. Keller, K. Petren and U. Reyer" for fieldwork help. Could you tell us a little more about who these people were and how they helped?
PG & RG: K.T. Grant is our daughter, Thalia. She helped us with fieldwork in many years, beginning in 1973 when she was six years old. Her help was crucial in 2005, when she visited Daphne to census the banded finches in order to find out which ones had survived and which ones had not. Rosemary and I could not visit the island that year because I had to have an operation for colon cancer, followed by a three-month course of chemotherapy under a doctor’s supervision. Thalia’s visit to the island was then followed by a longer visit by the other three helpers. Lukas Keller (University of Zürich) and Ken Petren (University of Cincinnati) had been post-doctoral fellows with me, and Uli Reyer was head of the Ecology Department at the University of Zürich, host on our two long visits to his Department, and a good friend. Their visit was nicely timed, fortunately, as heavy rain fell while they were there. Therefore we know the exact date when the drought ended. As it turned out, Thalia had found almost all the survivors on her short visit, and although our other helpers added very few to the list, their inventory gave us more confidence in our estimate of the true survival. In the next field season in 2006 we did not find a single banded finch that had escaped detection in 2005.
HS: Have you ever read this paper after it was published?
PG & RG: No, we have never read it, we have only checked some numbers in tables.
HS: Could you tell us why you decided to end fieldwork on this project in 2012?
PG & RG: We both retired from teaching at Princeton University in 2008. The last of our research money was spent in 2012, and after 40 years of fieldwork it seemed a good time to stop and the write a synthesis, which became the book Rosemary and I published in 2014: “40 Years of Evolution. Darwin’s Finches on Daphne Major Island.”