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This reprint is provided for personal and noncommercial use. For any other use, please send a request to Permissions, American Scientist, P.O. Box 13975, Research Triangle Park, NC, 27709, U.S.A., or by electronic mail to [email protected]. ©Sigma Xi, The Scientific Research Society and other rightsholders Adaptive Radiation of Darwin’s Finches

Recent data help explain how this famous group of Galápagos birds evolved, although gaps in our understanding remain

Peter R. Grant and B. Rosemary Grant

powerful metaphor for evolutionary relationships depart radically from Now is an opportune time to ad- Aary diversification is a tree. A typi- the orthodox view of an adaptive radia- dress these questions: Estimating the cal spreading tree has a single trunk, tion with one trunk, a few branches and structure of the evolutionary tree has two or more major branches, several many terminal twigs. The most striking become possible in the past few years minor branches and many twigs. Its difference from the idealized model is as a result of studies on DNA sequence foundations—its roots and the rem- that near the base of the tree, where the variation among the birds (Figure 3). nants of the original seed—remain main trunk—representing the ancestral The results ultimately compel us to hidden from sight. The metaphor ap- species—splits, only one of the result- reconsider the metaphor of a tree. plies to the full set of living things on ing trunks leads to several branches and Earth—“the tree of life”—as well as to many twigs (Figure 2, bottom). The other The Beginning of Radiation small groups of species, whether they trunk gives rise to little more than thin Darwin’s finches arose in South Amer- are marsupial mammals or Hawaiian twigs, although they have persisted in ica. The ancestors arrived on the Ga- Drosophila. We can think of the typi- growing to the crown. The next divi- lápagos islands by flying over water cal crown of a tree as resembling the sion is also asymmetrical. The third divi- for at least 1,000 kilometers. There shape of an umbrella, with twig-bear- sion is more orthodox, producing two has been little debate about these two ing branches radiating in all directions branches that radiate approximately points. The only credible alternative (Figure 2, top). The ends of the twigs equally, one yielding the ground finches is that the finches arose on Cocos Is- represent organisms adapted to sepa- and the other yielding tree finches. Nev- land, which lies 600 kilometers to the rate microenvironments; the tree over- ertheless, the tree as a whole is lopsided. northeast of the Galápagos, where a all represents an adaptive radiation. Even if a model fails to fit the data solitary species of Darwin’s finch still Darwin’s finches are a prime exam- perfectly, it is useful to describe evo- resides. Three years ago, molecular ge- ple of an adaptive radiation. Fourteen lutionary branching with a metaphor netic data eliminated that possibility; or perhaps 15 species, all derived from in mind, because the confrontation be- the data demonstrated a phylogenetic a common ancestor, occupy individu- tween data and metaphor encourages origin of the Cocos finch after an ini- al ecological niches to which they are the posing of sharp questions. Being tial evolutionary split among Darwin’s adapted, principally because of the size forced to fit data to an idealized concept finches on the Galápagos (Petren et al. and shape of their beaks in relation to may lead to new insights and revised 1999, Sato et al. 1999). It is now clear the food they eat. Yet on close inspec- idealizations. For example, as we dis- that ancestral finches first colonized tion, we now know that their evolution- cuss in more detail later, thinking about the Galápagos, then the populations the loss of lower branches in evolution- began to diverge, and only after that Peter R. Grant has been a professor of ecology ary trees forces us to consider past ex- did the Cocos finch species arise. A and evolutionary biology at Princeton University tinctions and the contribution of those warbler finch (Certhidea fusca, see Fig- since 1985. He was educated at the University of losses to the current form of a tree. ure 2) may have colonized Cocos Is- Cambridge, the University of British Columbia The concept of adaptive radia- land and evolved into the Cocos finch and Yale University, and previously taught tion raises four main questions in our there. Alternatively, the warbler finch at McGill University and the University of minds: Michigan. B. Rosemary Grant is a research scholar Figure 1. Finches of the Galápagos Islands with the rank of professor in the same department. Origins: Where did the ancestors come provide a classic example of adaptive radia- She was educated at the University of Edinburgh, from, when and how? tion, the process that leads to evolutionary Scotland and the University of Uppsala, Speciation: How and why are new spe- diversity. The finches, which include the Sweden, where she obtained a Ph.D. in 1986. cies formed? cactus finch Geospiza scandens, live in a Their work was profiled in Jonathan Weiner’s broad range of habitats and rely on diverse Diversity: Why are there x number of Beak of the Finch. Address: Department of food sources. The authors’ work has includ- Ecology and Evolutionary Biology, Princeton species? ed field experiments investigating how the University, Princeton, NJ 08544-1003. Internet: Disparity: Why are these species as dif- Galápagos finches are related to one another [email protected] ferent, or as similar, as they are? and how they have diverged.

© 2002 Sigma Xi, The Scientific Research Society. Reproduction 130 American Scientist, Volume 90 with permission only. Contact [email protected]. Fritz Pölking/Peter Arnold, Inc. © 2002 Sigma Xi, The Scientific Research Society. Reproduction with permission only. Contact [email protected]. may have given rise to the Cocos finch plumage and song of the Cocos finch seed-eaters. A recent survey of mito- (Pinaroloxias) on the Galápagos, with so closely resemble the next branch in chondrial DNA sequence variation the species colonizing Cocos island the finches’ evolutionary tree. among 30 candidate species and their later, eventually becoming extinct on The original ancestors of Darwin’s relatives has pinpointed the most like- the Galápagos. We favor the second finches have been identified as a group ly closest living relatives of Darwin’s of these possibilities because the black of South American birds known as finches—members of what are known as the grassquit genus Tiaris (Sato et Cactospiza Geospiza al. 2001). As for when the ancestors pallida magnirostris Geospiza arrived on the Galápagos, the differ- Cactospiza Geospiza scandens ence in mitochondrial DNA between heliobates fortis Darwin’s finches and the Tiaris spe- Certhidea Geospiza olivacea Certhidea cies suggests an approximate answer. Camarhynchus fuliginosa fusca The answer depends on the standard psittacula assumption that nucleotide changes Camarhynchus accumulate in mitochondrial DNA at pauper Geospiza a rate of 2 percent per million years. conirostris This assumption may not be exactly Camarhynchus parvulas true; studies of birds on Hawaii have detected a slightly slower rate of diver- insectivorous granivorous cactus-feeding gence of 1.6 percent per million years (Fleischer and McIntosh 2001). But Platyspiza Pinaroloxias inornata even at this slower rate, the origin of crassirostris Darwin’s finches would be no earlier than three million years ago. vegetarian Geospiza difficilis Youth and rapid diversification dis- Geospiza tinguish Darwin’s finches compared difficilis with other avian radiations on other tree finches ground finches warbler-like islands. Robert Fleischer and Carl Mc- Intosh (2001) have estimated that the ground finches famously diverse Hawaiian honeycreepers started diverging 6.4 million years ago. In the same archipelago five ancestral or more thrushes evolved in 4.2 mil- finch species lion years, three goose-like ducks called Moa-Nalos evolved in 4.3 million years, and four species of crows evolved in 5.2 Certhidea Certhidea Platyspiza million years. In all these cases the rate olivacea fusca crassirostris of species accumulation—that is, speciation minus extinction—was slower than among Darwin’s finches, as judged by the average time to double the existing number of species. Darwin’s finches have a doubling time of three-quarters tree finches vegetarian finch of a million years. Even the spectacular radiation of Hawaiian honeycreepers, which resulted in more than 50 species before the actions of humans decimated ground finches Pinaroloxias inornata the group, had a species doubling time that exceeded 1.0 million years. We know of no group of birds that has di- warbler finch versified faster than Darwin’s finches.

Formation of New Species warbler-like The central problem of adaptive radiation—indeed, of the origin of biological diversity in general—is the question of

Figure 2. Evolutionary trees attempt to represent how Darwin’s finches evolved. The balanced evolutionary tree (top) is an older representation suggested by David Lack; the ancestral unbalanced evolutionary tree (below) proves grassquit species more accurate. Because of asymmetry in the earliest divisions, the tree looks lopsided.

© 2002 Sigma Xi, The Scientific Research Society. Reproduction 132 American Scientist, Volume 90 with permission only. Contact [email protected]. how and why one species gives rise to two. For the radiation of Darwin’s finches, we gave one answer in this 14 grams magazine 21 years ago (Grant 1981). G. fuliginosa That answer was the allopatric model of speciation, a model first sketched by Leopold von Buch in 1825, inde- 20 grams pendently developed by Darwin and G. fortis Alfred Russel Wallace, elaborated by Theodosius Dobzhansky and Ernst Mayr, and adopted by almost all biologists up to and beyond the first mono- 35 grams graph on the evolution of Darwin’s G. magnirostris finches by David Lack in 1947. In the allopatric model of speciation, geographical separation (that is, 21 grams allopatry) promotes evolutionary diver- G. scandens gence. In the first step of this model as applied to Darwin’s finches, an ancestral species colonizes an island (Figure 28 4), say San Cristóbal, the island clos- grams est to the continent. The newly estab- G. conirostris lished population evolves by natural selection, becoming better adapted to 20 the prevailing conditions, as well as grams by genetic drift. In the second step, a G. difficilis few dispersers colonize a second island and adapt to the new conditions. 13 grams The geographically separated popula- C. parvulus tions diverge, and the process of island- hopping divergence may be repeated several times before two populations encounter each other again in sympat- 20 grams ry, the third step. C. psittacula The meeting of the two populations can result in three possible outcomes: interbreeding of members of the two 18 grams populations without a loss in fitness, C. pauper despite the genetic differences ac- quired during their separation; interbreeding with fitness loss, because of 18 grams the reduced viability of the offspring C. heliobates or because of partial sterility; or finally, no interbreeding. In the first case, there has been no speciation, whereas in the 21 third case, two species have formed grams C. pallida from one. The second case is the most interesting because it represents a stage in the process of speciation on the way to the reproductive isolation of one 34 grams species from the other. P. crassirostris The second case is unstable and can lead, in its turn, to three alternative 8 outcomes: increasing mixing of the grams C. fusca Figure 3. Phylogeny of Darwin’s finches was estimated using microsatellite DNA length variation (adapted from Petren et al. 1999 and 13 Grant 1999). The text also refers to the war- P. inornata grams bler finches (Certhidea), the medium ground finch (Geospiza fortis), the cactus finch (Geospiza scandens) , the Cocos finch (Pina- 9 grams roxias) and the sharp-beaked ground finch indicates male coloration C. olivacea (Geospiza difficilis).

92 66 70 53 57 63 0.1 100 93 81 83 speciation from a mass of particulars. COSTA RICA Much data support the model in the 92° W 2.0 case of Darwin’s finches. These data PANAMA include quantitative ecological data on Darwin Cocos the differences in food supply among 1.5° N islands, differences among species in feeding behavior and diets in relation Galápagos to beak sizes and shapes, as well as in- 1.5 Archipelago Wolf direct evidence of competition for food among species. Twenty-one years after ECUADOR we wrote about the allopatric model in this magazine, how does the model Pinta fare when confronted with new details 1.0 of the radiation of Darwin’s finches? Genovesa Marchena Ecology, Time and Change 0° Because of the proximity of the Galá- pagos islands, the finches can easily San Santiago travel among the islands. If two populations of one kind of finch diverge Daphne to a large degree, they should eventu- Major Baltra ally be able to coexist, and we there- Rábida fore expect to find them together on 1 Fernandina 3 the same island. In two respects we Pinzón now know that the allopatric model we proposed in 1981 (Figure 4) is wrong. Santa Cruz Santa Fe Neither error is fatal to the abstraction, 1° S 2 although each requires that the model San Cristóbal be modified. The first error is to sup- Isabela 2 pose that the initial speciation process gave rise to two species that came to live on the same island after a period of Santa Floreana 2 geographical separation. That is, spe- Española ciation does not require step 3 shown 91° W 90° W in the illustration. As indicated in our discussion of the trunk and branches Figure 4. Allopatric model of speciation proposes that species evolve by diverging on different of the Darwin’s finch tree, after the two islands (allopatry) and eventually coexist on the same island (sympatry). In step 1, immigrants from the mainland colonize the Galápagos. In step 2, which can occur repeatedly, the birds groups of warbler finches were formed disperse to other islands and become adapted to local food supplies. In step 3, populations from one, they apparently remained on of birds recolonize an island on which their ancestors lived. Many of these volcanic islands different islands. Similarly, the sharp- formed from a hotspot currently beneath Fernandina after the ancestral finches arrived from beaked ground finch populations have South America. remained geographically separated even though they have diverged mor- two populations despite reduced fit- study the process of speciation, but phologically to a large degree (Grant et ness of the hybrids until they have it presents a formidable challenge to al. 2000). In contrast, the more recently fused into one; divergence driven by those who seek a definition of species evolved ground finches and tree finch- natural selection, sexual selection or that has sharp boundaries, especially es have established sympatric popula- both, when the most different indi- if the criteria for distinguishing the tions in various combinations. These viduals of the two populations are species are to be solely genetic. observations are surprising in that favored over the most similar ones, Thus, as David Lack first pointed given enough time, populations are since the former are less likely to mate out in 1947, speciation of Darwin’s expected to diverge sufficiently to per- with members of the other popula- finches involves the evolution of sig- mit coexistence, and coexistence will be tion and suffer a loss of fitness and nificant ecological and reproductive achieved as a result of dispersal among because they are less likely to compete differences. Explaining the full radia- islands. Evidently there are constraints for the same resources; or the competition in terms of the allopatric model is on both divergence and dispersal, con- tive elimination of one population by accomplished by invoking a repetition straints that are probably ecological in the other, most likely, elimination of of the same speciation process several origin, and we suspect that they in- the new population by the incumbent, times, but with the species produced crease with the passage of time. unless the island is large and diverse differing according to the particular The second mistake was to assume enough to allow their coexistence in ecological circumstances that guided that all the islands existed at the outset. separate habitats. All these may take a each pathway. This is not a serious mistake because long time. The complexity of the out- The allopatric model is an abstrac- the islands we arbitrarily chose for il- comes is fascinating to biologists who tion designed to capture the essence of lustrating the model—San Cristóbal,

© 2002 Sigma Xi, The Scientific Research Society. Reproduction 134 American Scientist, Volume 90 with permission only. Contact [email protected]. Española, Floreana and Santa Cruz— 20 are all fairly old and were probably involved in the first speciation cycle. Exposure of the mistake nevertheless islands has far-reaching consequences for in- 15 terpreting the radiation. species Geological reconstructions of the archipelago over the three-million-year time period during which the finch radiation unfolded has established 10 that an increasing number of islands numbers formed volcanically in the region of a western hotspot and in the region of a northern spreading center. As the 5 number of islands increased, so did the number of finch species (Figure 5); we estimate the number of finch species by ignoring the unknown extinctions and 0 simply back-calculating from the esti- –5 –4 –3 –2 –1 0 mated ages of contemporary species. This new view of an adaptive radia- age (million years before present) tion taking place in a changing envi- Figure 5. Number of species of Darwin’s finches has increased as the number of Galápagos ronment is profoundly different from islands has increased (from Grant 2001). The accumulation of species reflects the results of the previous conception. It requires speciation minus extinction; only extant species were used to draw the curve. Conceivably, understanding how a changing envi- extinction exceeded speciation at one or more critical points in the history of Galápagos. ronment—differing numbers of islands, climate and vegetation—acts as a force driving the radiation. The Galápagos were probably not a diverse environment full of ecological opportunity for all 14 species of Darwin’s finches when the ancestral species arrived. Rather, the archipelago was much simpler; over three million years it grew in complexity and changed in character. The change in the character of the archipelago resulted, in part, from global cooling that started well before the on- set of the recent ice age about 2.8 million years ago and has continued to the present. The amplitude of temperature oscillations—and probably of precipita- tion—has increased in the past million years. These two climatic features probably affected the Galápagos vegetation, although there is no direct evidence for this. The ancestral finches arrived on the Galápagos at a time close to the on- set of the Ice Age, possibly aided by new wind patterns set up by changes in ocean circulation resulting from the closure, reopening and closure of the Panamanian isthmus. The original Ga- lápagos finches encountered an environment that was possibly like Cocos Figure 6. When Darwin’s finches colonized today—more equably warm and wet the Galápagos islands, they may have encoun- and less seasonal than the present cli- tered a rainforest habitat, such as now exists mate. Food resources also differed. The on Cocos Island (above and top right). The climate has changed in the past three million ancestral species changed in response, years. In Galápagos lowland habitats (for ex- acquiring a long and narrow beak better ample, on Genovesa island, bottom right), the suited to exploiting nectar and insects climate probably has become more arid, with and spiders, which we presume were vegetation and food sources changing as a re- common on Galápagos at that time. sult. (Photographs courtesy of the authors.)

© 2002 Sigma Xi, The Scientific Research Society. Reproduction 2002 March–April 135 with permission only. Contact [email protected]. rated geographically, like the warbler finches, we have no means of knowing whether they could interbreed, and with what consequences, under natural circumstances. We are left to construct the probable outcomes of natural encounters with artificial methods, such as, hypothetically, breeding them in captivity. On the other hand, there is no ambiguity about the reproductive connectedness of populations on the same island; therefore, we concentrate on them. Our long-term field studies of banded birds on Daphne Major (Grant 1999) and Genovesa (Grant and Grant 1989) reveal that sympatric species (those on the same island) belonging to the same genus do hybridize, albeit rarely. Re- duced fitness in hybrids is thought to Figure 7. In experiments to test finches’ response to song, the authors used a speaker mounted result from genetic incompatibilities ac- on a tripod and a tape recorder to play songs sung on other islands. Birds respond to the song of quired while the populations are sepa- their own species, which they learn from their fathers. (Photograph courtesy of the authors.) rated. Surprisingly, this expectation is not always realized on Daphne Major. Subsequently, speciation cycles were underlying variation in genetic factors. Sometimes hybrid individuals with beak influenced by the changing number of Offspring of the survivors had larger sizes intermediate between those of the islands, increasing seasonal aridity and beaks, on average, than did the popula- parental species suffer a disadvantage the resulting changes in the composi- tion before natural selection. because the particular seeds they are tion and distribution of vegetation, ar- A repeat performance of selection best suited to eat are rare. At other times thropods and food sources generally. and evolution took place nearly 10 the hybrids appear to be at no disadvan- years later when the island suffered a tage compared with the parents that pro- Observed Selection and Adaptation drought again, but the outcome was duced them. The fitness of the hybrids is In our 30 years of field work in the different. This time plants with larger a function of the environment; there is Galápagos, we have observed small- seeds suffered, and small seeds over- no evidence of a genetic barrier to hy- scale environmental changes that mir- whelmingly dominated the food sup- bridization. But perhaps that is because ror large-scale environmental changes ply, creating a selective advantage for not enough time has passed for such over the past three million years, lead- small birds with small beaks. Another barriers to evolve. Our long-term study ing to adaptive changes in beak size resident on the island, the cactus finch of medium ground finches and cactus and shape. Our studies have concen- (G. scandens) suffered less size-selec- finches has documented the passage of trated on the small island of Daphne tive mortality both times because it alleles between the two species. Major, where the residents are seed- depends less on seeds in its diet. These observations are valuable in eating ground ground finches. In 1977 Observing selection and evolution showing where it is not profitable to a drought prevented the regrowth of when environmental conditions fluctu- look for barriers to gene exchange: af- most of the seed-producing plants. The ate in the short term affects our views ter mating has taken place. Instead the population of medium ground finches of evolution in the long term. In the usual barriers arise before mating. Since (Geospiza fortis) declined in number in short term of a few decades, the oscil- different finch species have almost iden- inverse proportion to their size: Small- lations cancel out leaving the popula- tical courtship behaviors, the barriers beaked birds disappeared from the tion with a beak size that’s, more or must lie not in how courting individu- population at a faster rate than large- less, in dynamic equilibrium. Over the als act but in how they appear—wheth- beaked birds. The reason for the size long term of many decades, centuries er visually or acoustically. Related spe- selectivity was that after they had de- or even millennia as food resources cies are often distinguished by their pleted the supply of small seeds, the change, a vector of directional change beak sizes and shapes rather than their finches increasingly depended on the runs through the oscillations toward a plumage; they also sing different songs. remaining medium and large seeds. larger or smaller overall beak size, or Experiments with motionless stuffed Birds with large beaks could crack more pointed or blunt beak shape. specimens and other experiments with them open easily, whereas those with tape-recorded songs have demonstrat- small beaks could crack them only with Reproductive Isolation ed that both visual and acoustic cues time-consuming difficulty if at all. This As David Lack stated long ago, diver- elicit species-specific recognition from was a clear example of natural selection gence of reproductive traits leads to medium ground finches. that led to evolution in the next gen- the severing of a breeding connection Both male and female hybrids re- eration because the variation in beak between populations and, hence, to spond to the song type of their fathers size that we measure largely reflects an speciation. If populations remain sepa- when they choose a mate. Only males

© 2002 Sigma Xi, The Scientific Research Society. Reproduction 136 American Scientist, Volume 90 with permission only. Contact [email protected]. sing, and they sing only one type of fathers’ songs, a cultural analogue to Experiments that play tape-recorded advertising song throughout their lives. genetic mutation. Third and fourth, the songs of related but geographically sep- If pairs form between species, say be- frequency of newly arisen rare variants arated finch populations simulate what tween a female ground finch and a may increase either by chance or selec- would happen if birds from the sepa- male cactus finch, the offspring even- tively; a selective advantage may arise rated populations came together. They tually mate with members of their fa- if the songs transmit better in the new test the finches to see if they would re- ther’s species—in this case, other cactus environment (Bowman 1983), and as a spond to a song as if it were sung by finches. The sons will sing cactus finch result more effectively repel intruding a member of their own population, or songs, and the daughters will mate with males or attract females. The fifth rea- not. Although the conditions are arti- males singing cactus finch songs. son is close to the original Dobzhansky ficial, the experiments show that the Morphology also plays a role in mate idea: The mean frequency, its range and birds discriminate the alien song from choice. On Daphne Major, an excep- the trill rate of songs may change as that of their own species only when tional hybrid male that sang a cactus a passive consequence of changes in the songs differ substantially. Ongoing finch song but whose beak was closer either body size and hence the syrinx experimental research with warbler in shape to that of a medium ground (sound box) volume (Bowman 1983), or finches has so far found little evidence finch first mated with a cactus finch fe- changes in beak size (Podos 2001). But of discrimination, leading us to ques- male and later with a medium ground even related populations with similar tion whether the two forms (C. olivacea finch female. Thus, visual and auditory morphology and ecology, occupying and C. fusca) have reached the status of cues appear to act in association. acoustically similar environments—as separate species. But perhaps in natu- with the sharp-beaked ground finches ral circumstances, given enough time, Isolation by Song on Wolf and Darwin islands—can differ birds may learn to make finer discrimi- Perhaps the critical question for how profoundly in song (Grant et al. 2000). It nations. Nevertheless, the logical im- species form is this: How do cues that is difficult to escape the conclusion that plication is that in the past, there may guide mating decisions diverge in in- chance, in addition to selection, contrib- have been many such natural experi- cipient species and lead to reproductive utes to changes in song characteristics ments where the result was complete isolation? If beak morphology alone after a new island is colonized. intermixing, because the morphological were involved, the answer would be easy: Adaptation to local food resources in geographically separate regions raises reproductive barriers between populations even if they come together again. If this were the whole story, reproduc-

tive isolation would evolve as a passive fitness consequence or byproduct of ecological divergence caused by natural selection. This idea has a long history (Dobzhan- sky 1937), but song is also involved, beak shap e e body siz and song is a fundamentally different early trait because it is learned. In finches it is not under tight genetic control—as it is in insects such as Drosophila, crickets and lace-wing flies—although genetic factors may determine the limits of the sounds that the birds can learn and re-

produce. Experiments with finches in fitness captivity (Bowman 1983) and pedigree analyses (Grant and Grant 1989, 1996) have established that Darwin’s finches learn songs early in life from the father beak e shap and probably in conjunction with mor- late e body siz phological features. Early imprinting accounts for the mating pattern of hybrids according to paternal song type. Figure 8. In an adaptive landscape, peaks are regions of highest fitness for species that have The critical question should be re- the appropriate combinations of resource-exploiting characteristics. Peaks occur because food phrased: How do songs and responses resources are not distributed uniformly and because appropriate combinations of morpho- to them diverge in incipient species? logical characteristics can exploit the available resources most effectively. Natural selection leads to the ascent of a population to a fitness peak in an adaptive landscape. The heights and There is not one answer to this question positions of the peaks change with time, isolating one or more of the species from the others but five. First, the few individuals that or bringing them closer together in their traits. Speciation can take place by the sequential establish a population on a new island colonization of peaks (early). When the food environment changes, the adaptive landscape carry an incomplete range of songs or can change—for example, peak heights change, the depth between peaks change, or the peaks renderings of them. Second, sons may move either closer or away from each other to more isolated positions (late). The authors have produce random errors when copying observed the first two changes on Daphne Major (Grant 1999).

© 2002 Sigma Xi, The Scientific Research Society. Reproduction 2002 March–April 137 with permission only. Contact [email protected]. different populations to use the available resources effectively. Natural selection causes populations to ascend to fitness peaks in the adaptive landscape. The adaptive landscape has been made operational by using seed resources to construct maximum density profiles in relation to beak sizes of the seed-eating species of Darwin’s finches. Mean beak sizes of these species on 16 beak shape islands were then predicted from peaks in the expected density profiles (Schluter and Grant 1984, Schluter et al. 1985), with two main results. First, no more than one species was associated with a peak. Sec- ond, with few exceptions the association mainland between predicted and observed beak relatives sizes was tight. One factor affecting the body size closeness of fit was the presence or ab- sence of a similar competitor species. We 1 million are encouraged to think that with com- years ago plete knowledge of the food resources on the Galápagos islands, we might find CerC rthidead at least 14 peaks, and by their spacing 1.5 million better understand why the species are years ago as different from one another as they Geospiza are. We have not attempted to obtain difficilis Pinaroloxias anything close to a complete quantita- e

p inorin natan t tive knowledge of food resources on the islands because of the difficulty of com- bining, in one analysis, the full range of eak sha

b resources exploited by Darwin’s finch treet e species. The birds consume seeds, fruits, 2.0 million groundg u finnchesn e nectar, pollen, blood from seabirds and years ago finchesi hess from sea-lion placentae, caterpillars, spiders, insect larvae hidden beneath the bark of trees or in the tissues of leaves, Platyspiza mainlanda a d crassirostris and several other things (Grant 1999)! relatives Instead, we have developed a two- dimensional diagram (Figure 9) that body size attempts to show how the full range Figure 9. Graphs charting the morphological diversification of Darwin’s finches are similar to of Darwin’s finch beak morpholo- top-down views of the adaptive landscapes shown in Figure 8. These phylomorphologies show gies evolved, without regard to the the time course and directions of morphological changes with the approximate timing indi- unknown resource distributions that cated by the broken lines. In both graphs, body sizes increase to the right, and beak shapes determine fitnesses. An initially slow become increasingly pointed toward the top. The simple graph at top shows the diversifica- exploration of one part of the total mor- tion that would have been expected without environmental change. The bottom graph depicts phological space was followed by rapid the actual, observed changes. exploration of the remainder with re- and song differences between the pop- landscape (Figure 7). Sewall Wright first peated reversals in direction. The con- ulations had not become sufficiently developed the idea in terms of genotype trast between early and late may be large to allow a new and independent frequencies; G. G. Simpson then ex- more apparent than real if large birds population to become established on tended it to phenotypes—or the physi- with blunt beaks evolved early but the island. Such may have been the case cal manifestations of inherited traits were then competitively replaced by with the two groups of warbler finches. (Schluter 2000). The idea is to represent more efficient, newly evolved species. variation in two morphological charac- It is highly unlikely that fitness peaks Numbers and Differences of Species teristics that affect resource use along existed on the Galápagos islands for Another easily constructed metaphor two axes of a landscape. The third, verti- each of the 14 current species when the can explain patterns of diversity and cal axis represents fitness. Fitness peaks single ancestral species arrived. Peaks disparity in terms of environmental re- occur in the landscape because of the increased in number when new plants sources, principally food. However, few distribution of food resources and be- and arthropods arrived. As resources relevant data are available to test it. The cause of favorable combinations of mor- increased, decreased or changed in pro- concept is an adaptive topography or phological characteristics that permit portions, peaks increased or decreased

© 2002 Sigma Xi, The Scientific Research Society. Reproduction 138 American Scientist, Volume 90 with permission only. Contact [email protected]. in height, shifted in position, were de- rienced recently. This fact and the likeli- Cactus Finch of the Galápagos. Chicago: Uni- formed by accretion of new resources hood of extinction mean that the parts versity of Chicago Press. to existing peaks, became established in of the tree that formed early on cannot Grant, B. R., and P. R. Grant. 1996. Cultural new locations or disappeared altogeth- be entirely known in terms of what we inheritance of song and its role in the evolu- er, taking their finch occupants with can discover about recent speciation in tion of Darwin’s finches. Evolution 50:2471– 2487. them or precipitating their extinction. current environments. Understanding This dynamic view of Galápagos the base of the tree requires knowing Grant, P. R. 1981. Speciation and the adaptive radiation of Darwin’s Finches. American Sci- adaptive landscapes raises questions the particulars of how the environment entist 69:653–663. that cannot be answered with present has changed through time. Grant, P. R. 1999. Ecology and Evolution of Dar- data, among them: To what extent were Adopting metaphors like the evolu- win’s Finches. Princeton: Princeton Univer- adaptation, speciation and extinction tionary tree is a useful way to organize sity Press. impelled by environmental changes in information and to suggest new insights, Grant, P. R. 2001. Reconstructing the evolution the past? Have unrecorded extinctions but it can have a strong potential to mis- of birds on islands: 100 years of research. deprived us of evidence showing how lead when interpreted too literally. G. G. Oikos 92:385–403. species became isolated on peaks? Once Simpson’s famous metaphor of evolu- Grant, P. R., and B. R. Grant. In press. Lack of a species became adaptively special- tionary diversification being a process of premating isolation at the base of a phylo- ized on an isolated peak—for example, filling the “ecological barrel” nicely cap- genetic tree. American Naturalist. warbler finches—how did a portion of tures the importance of ecological oppor- Grant, P. R., B. R. Grant and K. Petren. 2000. The allopatric phase of speciation: the its population break out of its special- tunity in speciation, but misleads us into Sharp-beaked Ground Finch (Geospiza dif- ization straightjacket and give rise to thinking the environment has a fixed ficilis) on the Galápagos islands. Biological a new species? Are there peaks that re- and unchanging capacity for accommo- Journal of the Linnean Society 69:287–317. main unoccupied because they are too dating species. Meanwhile, the meta- Lack, D. 1947. Darwin’s Finches. Cambridge: far from existing peaks or because there phor of an evolutionary tree, although Cambridge University Press. has been insufficient time to occupy obviously valuable, deflects us from Petren, K., B. R. Grant and P. R. Grant. 1999. them, with previous occupants perhaps seeing that species hybridize—branches A phylogeny of Darwin’s finches based becoming extinct recently? Are parts anastamose—and that the ancestors of on microsatellite DNA length variation. Proceedings of the Royal Society of London B of the landscape composed of ridges modern species may have become ex- 266:321–329. rather than peaks (Schluter 2000), occu- tinct without their derived species do- Podos, J. 2001. Correlated evolution of mor- pied by more than one species spaced ing so—the “supporting” branches have phology and vocal signature structure in apart along the ridge by competitive or fallen. A metaphor that avoids these two Darwin’s finches. Nature 409:185–188. other interactions? unrealistic features is a river that divides Sato, A., F. Figueroa, C. O’hUigin, P. R. Grant, several times as it runs across a land- B. R. Grant, H. Tichy and J. Klein. 1999. Phy- The River of Life scape. This is closer to the metaphor of logeny of Darwin’s finches as revealed by Two decades ago, we applied the allo- an adaptive landscape than a tree is, and mtDNA sequences. Proceedings of the Nation- al Academy of Sciences USA 96:5101–5106. patric model of speciation to Darwin’s has the interesting implication that spe- finches, and tested and illustrated it with ciation—the evolution of isolated gene Sato, A., H. Tichy, C. O’hUigin, P. R. Grant, B. R. Grant and J. Klein 2001. On the origin data from studies on ground finches— pools (another metaphor)—requires spe- of Darwin’s Finches. Molecular Biology and representing some of the twigs and mi- cial, rare and perhaps capricious circum- Evolution 18:299–311. nor branches of the finches’ evolution- stances, like floods. Schluter, D. 2000. The Ecology of Adaptive Radia- ary tree. Now, with an estimate of the tion. Oxford: Oxford University Press. shape of the tree available from DNA Acknowledgment Schluter, D., and P. R. Grant. 1984. Determi- studies, we have examined the causes The authors thank Ken Petren for useful nants of morphological patterns in commu- of the adaptive radiations at the level of discussion, and for his help with both field nities of Darwin’s finches. American Natural- the trunk and major branches. For this, and lab work. ist 123:175–196. we have adopted a principle of evolu- Schluter, D., T. D. Price and P. R. Grant. 1985. tionary uniformitarianism, analogous Bibliography Ecological character displacement in Dar- win’s finches. Science 227:1056–1059. to the principle of geological uniformi- Bowman, R. I. 1983. The evolution of song in tarianism of James Hutton and Charles Darwin’s Finches. In Patterns of Evolution in Lyell. In essence the principle we start- Galápagos Organisms, ed. R. I. Bowman, M. Berson and A. E. Leviton. San Francisco: ed with is that the branches of today American Association for the Advancement were the twigs of yesterday and that of Science, Pacific Division, pp. 237–537. the processes of adaptation and specia- Dobzhansky, T. 1937. Genetics and the Origin Links to Internet resources for further tion occurred uniformly throughout the of Species. New York: Columbia University exploration of “Adaptive Radiation of tree. However, extending the patterns Press. Darwin’s Finches” are available on the of recently formed twigs backward Fleischer, R. C., and C. E. McIntosh. 2001. Mo- does not fully account for the patterns lecular systematics and biogeography of the American Scientist Web site: of the branches. Some twigs persist for Hawaiian avifauna. Studies in Avian Biology 22:51–60. In Evolution, Ecology, Conservation, http://www.americanscientist.org/ a very long time as twigs without ever and Management of Hawaiian Birds: A Vanish- becoming branches. Part of the reason ing Avifauna, ed. J. M. Scott, S. Conant and articles/02articles/Grant.html for this is that the environment early in C. van Riper, III. Kansas: Allen Press. the history of old twigs differed from Grant, B. R., and P. R. Grant. 1989. Evolutionary the environment that twigs have expe- Dynamics of a Natural Population: the Large