Plenary What Darwin’s Finches Can Teach Us about the Evolutionary Origin and Regulation of Biodiversity B. ROSEMARY GRANT AND PETER R. GRANT Darwin's finches on the Galépagos Islands are particularly suitable for asking evolutionary questions about adaptation and the multiplication of species: how these processes happen and how to interpret them. All 14 speces of Darwin's finches are closely related, having been derived from a common ancestor 2 million fo 3 million years ago. They lve in the environment in which they evolved, and none has become extinct as a result of human activity. Key factors in their evolutionary diversification are environmental change, natural selection, and cultural evolution. A long-term study of finch populations onthe island of Daphne Major has revealed that evolution occurs by natural selection when the finches food supply changes during droughts. Extending this finding tothe past, we discuss how environmental change has influenced the opportunities for speciation ‘and diversification of finches throughout ther history: The number of islands has increased, the climate has cooled, and the vegetation and food supply have changed, Keywords: adaptation, natural selection, speciation, song learning, Galipagos history jologists are increasingly interested in diversity. ]One major source of interes is the conservation of bio- diversity ina world threatened with anthropogenic habitat de- struction and environmental pollution. A second major source of interest isthe regulation and maintenance of existing biodiversity by natural processes and the functioning of this biodiversity in units that vary from small communities to large ‘ecosystems. Finally, the biodiversity puzzle has.a third piece, without which our understanding is bound to be incom- plete: the evolutionary origins of diversity. Reduced to simplest form, this is the Darwinian question of how new species arise and multiply. This question is the main focus of thisarticle, and we illustrate our points with Darwin's finches of the Galapagos Islands. Some organisms are unusually suitable for answering par: ticular questions. The squid, for example, has served neuro- biology well because it has a giant axon; Drosophila species have contributed much to cytogenetics because of the giant chromosomes in their salivary glands; and Arabidopsis, Caenorhabdites, and a few other small organisms have been ‘well chosen to investigate the construction of entire genomes. Darwin's finches are particularly suitable for asking evolu- tionary questions about adaptation and the multiplication of species: how these processes happen and how to interpret them. All species of Darwin's finches are closely related, having derived recently (in geological terms) from a common ancestor. They live in the largely undisturbed environment in which they evolved, and none has become extinct as result of human activity. Consequently, whatever we can learn about their ecology and evolution gives us insights into the process of speciation under entirely natural conditions. Pop- ulations of the same species occur on different islands, and in some cases they have different ecologies. This allows us to investigate the reasons for their divergence. Closely related species occur together on the same island and differ. This allows us to investigate the nature ofthe reproductive barrier between them and the question of how and why species stay apart. Thus, considering populations across the entire archi- pelago, we can see all stages of the speciation process, from start to finish, at the same time. In this article we survey the evidence from field studies of the ecological causes of diversification, The explanation for 2B. Rosemary Gran (e-mail pgrant@princeon.du sa senior research scholar «and professor in the Department of Ecology and Evolutionary Biology, and Peter R. Gratis theClass of 1877 Profesor of Zoolgy at Princeton Universi, Princeton, NJO85440, They have studied the eolgy, behavior, biogeography, «nd genetics of Darwin’ finches for he last 30 yars. Thi artic isan expanded version of a plenary address delivered atthe 53rd annual meeting of the American Institute of Biological Sciences, held in Arlington, Virginia, 22-24 March 2002. The vit ofthe symposium was “Evolution Understanding Life on Barth” © 2003 American Institute of Biological Sciences October 2003 / Vol. 53 No, 10 + BioScience 965LC LEE ETL EEL NOE IES I diversification involves natural selection, genetic drift, intro- gressive hybridization, and genetic as wel as cultural evolu- tion. Linking all these factors are the frequent and strong fluctuations in climatic conditions, between droughts on the one hand and extremely wet (El Nifio) conditions on the other, An important conclusion of this study is that environmental change is an observable driving force in the origin of new species. Using information from the study of contemporary finches, we then turn to questions of how and why their adaptive radiation unfolded in the way that it did. We focus on how environmental change in the past has guided the multiplication of finch species. Whereas the ‘microevolutionary principles were probably the same through- ‘out the finches’ radiation, the circumstances differed in important ways at different times. General principles coupled with specific circumstances explain the particular features of the radiation, The pattern of adaptation Atleast 14 species of Darwin's finches were formed in the last 2 million to 3 million years in the Galapagos archipelago and on Cocos Island. They stand as a model of adaptive radiation, that is, the production ina short period of time of many species from one occupying different ecological niches (Schluter 2000). Figure 1 shows the four points of the Darwin's finch compass to illustrate the finches’ diversity, and figure 2 shows three closely related species to illustrate how similar the intervening species are. That similarity makes it relatively easy to reconstruct the evolutionary transition from ‘one species to another. Darwin (1842) wrote about this phe- nomenon 7 years after he, FitzRoy, and their assistants collected the first specimens:“The most curious fact is the perfect gra~ dation in the size of the beaks of the different species of Geospiza.... Seeing this gradation and diversity of structure in one small, intimately related group of birds, one might fancy that, from an original paucity of birds inthis archipelago, one species has been taken and modified for different ends” (p.458). ‘Translated into the modern language of evolutionary bio- logy, “modified for different ends” means adaptated by nat- ural selection (figure 3). The modern evidence for this begins with an association between beak size and diet (Lack 1947, Bowman 1961). There isa strong relationship between the beak sizeof ground finch species and the maximum size and hardness of the seeds that the birds can crack (figure 4). The association between beak size and diet is most obvious when comparing the species that have contrasting morphology, such as the insectivorous small warbler finches (about 8 ‘grams [g]) and the granivorous large ground finch (about 30 8g). It i less obvious when comparing populations of the ‘same species on different islands. Nevertheless, different pop- Ulations of the sharp-beaked ground finch, Geospiza difficlis, feed in different ways on different foods with beaks of different size and shape. On the high islands of Santiago, Fernandina, and Pinta they have relatively blunt beaks and feed on arthro- pods and mollusks, as well as fruits and seeds in the dry 966 BioScience + October 2003 / Vol. 53 No. 10 season. On the low island of Genovesa, where their beaks are ‘much smaller, they ate more dependent on small seeds, as well as on nectar and pollen from plants, including the Opuntia cactus. Apparently uniquely on the low island of Wolf, they exploit seabirds (boobies, Sula spp.) in two dramatic ways. First, they kick the booby eggs until the eggs fall or hit a rock and crack, enabling the finches to open them and consume the contents. They also inflict wounds at the base of the sitting boobies’ wing feathers and consume the blood. On this island the finches’ beaks are long. In contrast to the sharp-beaked ground finches, birds with large robust beaks, such as the large tree finch, Camarhynchus psittacula, do not probe Opuntia flowers or poke at eggs. Instead, the beak of this finch is a tool for tearing bark and crushing twigs and small branches—a beak modified for a different end. These examples illustrate some of the ways that Darwin's finches vary in beak morphology and are versatile in their feeding habits. This versatility is fostered by ecological opportunity and impelled by food scarcity in the dry season and in dry years. Asevidence of adaptive diversification, associations like this do not satisfy everyone, because causality can be argued from beaks to diets as well as from diets to beaks. For example, can be said that finches feed in different ways because they have different beak sizes and shapes (e.g., Newton 1967). They surely do, but this begs the question of why the species’ beaks differ inthe first place. Another objection has been raised on the grounds of insufficiency of evidence. When David Lack (1947) argued that evolution had caused the fit between birds’ beaks and their food, an ecologist commented, “The problem, for instance, of whether certain specific characters (c.g. beaks of Geospizinae) are or are not adaptive (vague term) is one involving studies of field populations, genetics, and variation. It isa problem which might be largely solved by teams of workers dealing for a number of years with a par- ticularly favourable example. It is not one, I think, which can be settled in a four months stay, even if supplemented by the examination of skins in museums” (Richards 1948, p. 84). Without knowing about this critique atthe time, we picked up the challenge 30 years ago. Over the years the team consisted of lan Abbott, Peter Boag, Trevor Price, Lisle Gibbs, several assistants, and ourselves. Our study took place on the island of Daphne Major—a particularly favorable location, although one would not think so judging from its steep topography (see the photograph on p.970).. Adaptation as a process By virtue of its small size (0.34 square kilometers (km]), moderate degree of isolation (8 km from the nearest island), undisturbed habitat, and resident populations of finches, Daphne Major is a particularly favorable location for study- ing Darwin's three essential ingredients of adaptive evolution: variation, inheritance, and selection. We accomplished this by capturing and measuring many finches to determine pheno- typic variation, comparing offspring with their parents to determine inheritance, and following their fates across yearsFB C. olivacea 109 G. magnirostris 35 9 Figure 1. Four points of the Darwin's finch compass. Species with contrasting morphology (Certhidea olivacea, Geospiza difficilis, Geospiza magnirostris, and Platyspiza crassirostris) show the range of sizes and shapes in beaks, from small to large and from blunt to pointed. Photographs: B. Rosemary Grant and Peter R. Grant. to detect selection. We found pronounced heritable variation in beak size and body size within populations of the medium ground finch (Geospiza fortis) and the cactus finch (Geospiza scandens). We also found that when the environment changes, some of the variants in each population survive while others die. This amounts to a vindication of David Lack’ views on adaptation, Birds with small beaks and small body size suffered selec- tive mortality in 1977, during a severe drought (figure 5). The larger members of the medium ground finch population survived on a diet of large, hard seeds, which increasingly dominated the food supply asa result of an initial preferen- tial consumption of small seeds. Smaller birds, lacking the ‘mechanical power to crack the large seeds of Tribulus cistoides and Opuntia echios, died at a higher rate than large birds. An evolutionary response to directional natural selection followed in the next generation (figure 5), because beak size variation is highly heritable (Keller et al. 2001). Natural selection in the opposite direction, with small birds surviving disproportionately, occurred 8 years later. ‘The island experienced a major, prolonged El Nifio event from November 1982 to August 1983. The abundant rain and high temperatures transformed the vegetation and food sup- ply of the finches, and they bred for 8 months as opposed to the usual | or 2 months. Vines and other plants multiplied and P. crassirostris 349 G. difficiis 20 9 Plenary | Figure 2. Three recently evolved | species of Darwin's finches (Geospiza fuliginosa, Geospiza fortis, and Geospiza magnirostris) differ principally in size, but also in beak shape. Photographs: B. Rosemary Grant and Peter R. Grant. spread, smothering the low-growing Tribulus plants and Opuntia cactus bushes. The seed supply became dominated by small seeds, and seeds of Tribulus and Opuntia became scarce, When the island entered the next drying-out episode during the drought of 1985, the supply of seeds fell, and so did the numbers of finches from high points in the produc- tive years of 1983 and 1984. Large birds died atthe highest rates hence, the medium ground finches that were small, with rel- atively pointed beaks, were selectively favored. ‘Thus selection oscillates indirection. We have observed this repeatedly over the full 30-year period (Grant and Grant 2002a). Asa consequence, neither the medium ground finch nor the cactus finch has remained morphologically constant orsstatic. In fact, the mean body size and beak shape of the two species are not the same now as they were at the beginning of the study (figure 6). In an environment subject to climatic and floristic change, the finches have changed (evolved). We have directly observed the sort of adaptive change that is normally only inferred from a comparison of related popu- lations differing in mean morphology. ‘Summarizing, this study has taught us four things about natural selection: ‘+ Itisan observable, interpretable, and repeatable process in a natural environment. ‘October 2003 / Vol. 53 No. 10 + BioScience 967Plenary Speciation begins with the divergence of a population and is completed when two pop- ulations that have diverged on different islands establish coexistence with little or no inter- breeding (Mayr 1942, Grant 2001). We ‘obtained insight into the initial process of divergence on Daphne Major, thanks to a highly fortuitous circumstance: the founding of a new population, ‘The large ground finch (Geospiza magni- rostris) became a breeding member of the community in late 1982, when two females and three males began to breed. In preceding years we had observed immigrant members of this species on the island in the dry season, but when the rains began they disappeared, presumably returning to their island of origin to breed. Not so in El Nifio! The breed- ing birds produced 17 fledglings in 1982— 1983, but only one of the breeding pairs produced the next generation. A daughter bred at different times with two brothers, ‘one of which can be ignored because the | _ offspring did not survive to breed. Thus, the population was effectively founded by a single pair, and the next generation com- prised a sister-brother pair. We have followed the fate of this population ever since (Grant et al. 2001). There are now 30 to 40 breeding pairs on the island, Observations of a newly founded popu- lation go to the heart of the question of how biodiversity generation begins. Environ- ‘mental change appears to have been a key factor in facilitating population establish- ment and subsequent exponential growth. y Figure 3. The intergradation of beak sizes and shapes, illustrated with outlines . 1-3, Geospiza magnirostris; 4-7, Geospiza conirostris; 8-13, Geospiza fortis; 14-15, Geospiza fuliginosa; 16-21, Geospiza difficilis; 22-24, Geospiza scandens. Illustration by Swarth of the six species inthe genus Geosp (1931), from Abbott and colleagues (1977). * toscllates in direction, ‘ Ithappens when the environment changes. ‘+ Ithas evolutionary consequences (adaptive change). Almost 100 years after Darwin's visit to the Galapagos, a systematis, Harry Swarth, came close to suggesting that evo- lution was not over and done with but could actually be witnessed when he wrote that “the extraordinary variants that crop up in a series [of museum specimens] give an im- pression of change and experiment going on” (Swarth 1934). Based on the evidence of Darwin's finches, evolutionary changes are indeed going on. 968 BioScience + October 2003 / Vol. 53 No. 10 ‘The G. magnirostris population experienced a genetic bottleneck (microsatellite allelic diversity fell), and inbreeding depression occurred, as shown by the relatively poor survival of the 1991 cohort. Small additional changes were caused by natural selection on beak morphology and probably by genetic drift, All of this is to be expected, but some other features ‘were surprising. Immigration did not occur just once but repeatedly, especially in the 1990s. With one exception, im- ‘migrants that stayed to breed came not from the obvious and closest potential source (Santa Cruz Island) but mainly from one farther away (Santiago), as revealed by their micro- satellite DNA. A major change took place in the frequency of song types in the population. This change was initiated by a single male that bred for the first time in 1991. In addition to this nongenetic, culturally transmitted contribution, he introduced a total of 11 new alleles at the 16 microsatellite loci surveyed.ne Log beak depth Figure 4. As the average beak depth of a population of _granivorous Geospiza species increases, o does the maxi- ‘mum size and hardness of the seeds they can crack. Based (on Schluter and Grant (1984). Thus, while environmental change was the key factor that triggered the founding of a new population, some idiosyn- cratic genetic and nongenetic factors determined the fate, de- velopment, and composition of the population, Even though ‘one individual made a large contribution to the population, overall changes were relatively small in magnitude, for three reasons: Selection pressures were weak, the population did not remain small enough for random genetic drift to be effective, and continuing immigration would have retarded diver- gence. If the case of G. magnirastris can be considered repre- sentative of how speciation begins, we would have to conclude that it starts slowly, with small steps. Speciation: The end Speciation is completed when two populations that have diverged in allopatry can coexist with little or no inter- breeding. Medium ground finches and cactus finches ‘occupy different ecological niches, although their diets over- lap. The ecological differences presumably permit coexistence in sympatry, in an environment (e.g., Daphne Major) whose food supply fluctuates in abundance and composition. To paraphrase David Lack (1947), the species are ecologically isolated through niche differences that evolved by natural selection in allopatry. The differences may have been enhanced by selection in sympatry, thereby reducing inter- specific competition for food. But how do the species maintain coexistence without interbreeding? What are the dif- ferences that keep them reproductively isolated, and how did the differences evolve? Members of the group of closely related ground finch species do not differ in plumage or courtship behavior, but they do differ in beak morphology, and they differ conspic- uously in song (Grant 1999). These two sets of cues, visual and vocal, have been shown in separate field experiments to be used by finches in discriminating between their own and ° 1976 Offspring | | os 2 is. 5° | Bo = tea * 1978 Offspring . 7378 88 93) 98 103 8 1B : Beak depth Figure 5. Evolutionary change in beak depth in the popu- lation of Geospiza fortis on the island of Daphne Major. The upper panel shows the distribution of beak depths in the breeding population in 1976, with the survivors of the 1977 drought that bred in 1978 indicated in black. The difference between the means, indicated by a caret, isa ‘measure of the strength of natural selection. The middle and lower panels show the distributions of beak depths of fully grown offspring hatched in 1976 and 1978, respec~ tively. Evolutionary change between generations is mea sured by the difference in mean between the 1976 popula- tion before selection and the birds hatched in 1978, other species (Ratcliffe and Grant 1983a, 1983b, 1985). Thus, part of the answer to the question of reproductive isolation is that itevolvesasa consequence of adaptive evolution of beak sizes and shapes in allopatry. The other part, centered on song, is more complex. ‘Song differences play a major role in keeping species apart. Like beak differences, song differences presumably arise through divergence in allopatry for reasons that are not en- tirely clear. Songiis an interesting trait because it is culturally, and not genetically, inherited. We know this from a few October 2003 / Vol. 53 No. 10 + BioScience 969Plenary @aemanmmmasemasmmnenmesnesannasssERNAAN I Daphne Major, a volcanic remnant in the Galapagos archipelago, is the site of the ‘authors’ long-term study of evolution in Darwin's finches. Photograph: David Parer. experiments with captive birds (Bowman 1983), supple- mented by field observations of songs of offspring, parents, and even grandparents (Grant and Grant 1989, 1996). Only males sing an advertising song; it is simple and is sung un- altered throughout life, which may be as long as 16 years. Most sons sing the same song subtype as their fathers, while a minority sing a different song subtype that is sung by other male members of the same population. Thus, song is acquired through learning early in life in a process that resembles imprinting; it is generally acquired from fathers during the period of parental dependence, in association ‘with parental morphology. By their pairing patterns, females give evidence of learning songat the same time and from the Rare exceptions to these rules provide additional valuable information on the role of learning and its bearing on the ‘question of what keeps species apart. Once again, environ- mental change associated with an El Nifio event has pro- vided crucial information, Medium ground finches and ‘cactus finches hybridize rarely. Before 1983 the hybrids died without breeding, at a time when most of the “pure” species produced in the same years also died without breeding. The EI Nifio event of 1983, resulting in an abundance of small seeds, altered the environment in a way that was favorable to the survival of the hybrids. The hybrids that were produced in 1983 backcrossed to medium ground finches in 1987, and others that were produced in 1987 backcrossed to cactus finches in 1991. The direction of backerossing differed because in 1983 the hybridizing male was a cactus finch that sang a ‘medium ground finch song, whereas in 1987 the hybridizing males were cactus finches that sang cactus finch songs. Sons of all families sang the same song as their fathers, and daughters in each case mated with males that sang the same song type as their fathers. 970 BioScience + October 2003 / Vol. 53 No. 10 Hybridization is sometimes the re- sult of heterospecific singing through apparent misimprinting. The causes of misimprinting and hybridization are idiosyncratic and difficult to determine. They include extra-pair mating, interspecific takeover of nests with eggs, and dominant singing of a lose neighbor. Ecologically, the sig- nificant feature is a change in the environment that has facilitated the introgression of genes. F, hybrid and backcross survival is not intrinsically lower than the survival ofthe parental species, and there i no sign of dimin- ished fitness when hybrids breed. In fact, in the 1990sand up to the present, the flow of genes from the medium ground finch to the cactus finch population has contributed to a decrease in mean body size and a blunter beak morphology of cactus finches (Grant and Grant 2002a). The barrier to gene exchange ‘erected by song differences has been breached, and environ- mental change appears to have been the most important factor. ‘To summarize, the coexistence of finch species is facilitated by divergence in beak morphology and song. Beaks diverge under natural selection, but why songs diverge is less clear. Cul- tural drift, a process of random change in culturally trans- mitted (learned) traits, is probably involved, and sexual se- lection may be involved as well. The end point of speciation. is the complete absence of gene exchange. Many, if notall,co- existing populations of Darwin's finches have not quite reached that point, although they function as species by re- ct even in the face of occasional gene exchange. ers two important lessons. Firs, species diverge in mate preferences before genetic incompatibilities evolve. Second, different populations can function as biological species before they would be recognized as species solely on the basis of ge~ netic distinctness. History: The initial colonization The present is known; the past is inferred. To understand the past of Darwin’ finches, the first question that needs to be ad- dressed is when the radiation began, because the answer sets the boundary on relevant Galipagos history. In the absence of fossils, genes are our best source of information about this history (Price et al. 2000), The closest genetic relatives of Darwin’s finches on the South American continent, in Central America, and in the Caribbean are a group of seed- caters (Tiaris and relatives) allied to tanagers (Sato etal. 1999, Burns et al.2002). Darwin's finches diverged from them in the last 2 million or possibly 3 million years, according to caleu- lations based on an assumed molecular clock applied to mitochondrial DNA and allozyme data (Grant 1999). Thea Plenary G. scandens Large PC1 beak shape ‘Small 1970 1980 ©1990-2000 1970 1980 1990-2000 Pointed PC2 beak shape Biunt 1970 1980 1880 +2000 Year | 9 | s mu, |B AS 1970 1980 ~—-1990 +2000 Year Figure 6. Changes in the beak size and shape of Geospiza fortis and Geospiza scandens on the island of Daphne Major. Mean trait values for each year are indicated by solid circles, and 95% confidence intervals are shown by vertical bars above and below the mean. In the absence of change, the means should remain within the 95% confidence intervals (horizontal broken lines) of the mean estimates {from the 1973 samples. PC refers to pi “ipal component, obtained from a principal components analysis of size and shape variables, From Grant and Grant (2002a). recent origin of Darwin's finches helps to explain why they are still capable of exchanging genes. Divergence from their mainland relatives began when the finches colonized the Galapagos islands. Situated 900 km from continental Ecuador on the Nazca plate and moving imperceptibly toward the mainland, the archipelago isa re- mote place for birds to visit. Colonization is an improbable event, Nevertheless, according to one calculation, ancestral Darwin's finches arrived in a moderately large flock (or several small ones). Modern finches are genetically diverse at the major histocompatiblity complex locus, and Vincek and colleagues (1996) used the allelic diversity of class II genes to calculate that the original colonists numbered at least 30 individuals. Improbable events may arise in improbable and hence rare circumstances. What might those circumstances have been? Any answer must be speculative, even if rooted in current phenomena. The circumstances that promote dispersal of contemporary finches within the Galipagos archipelago are (a) high finch density following prolific breeding in El Nino years and (b) forest fires caused by volcanic eruptions. Ifthe unusual dispersal activity from the mainland followed sim- ilar patterns, it may have been induced by unusual voleanic activity in the Andes. Burning of the forests in one such episode would be followed by the establishment of large areas of shrub and secondary growth. With the buildup of finch populations in secondary forest, and another round of fires and burning, large numbers of finches and other birds in coastal regions would ly out to sea to escape the flames and smoke. The colonists would be helped if mats of vegetation ‘were rafted out to sea by strong El Nino-associated flooding from the Guayas River. Global temperatures were warmer 2 million to 3 million years ago, and permanent El Nifio con- ditions are thought to have occurred until about that time (Cane and Molnar 2001). The most marked shift in climate seems to have occurred at 2.4 million to 2.5 million years ago. This may be when the ancestral Darwin's finches arrived. Relevant history of the Galapagos ‘To understand the past, the second question that needs to be addressed is how the islands have changed, ifat al, since the first finches arrived. The simplest possible answer would be October 2003 / Vol. 53 No. 10 + BioScience 971PLY EZ-_AMAAAA . | ° | om s Bw 2 € 5 Zs. q 5 5 i Age MY before present — Figure 7. The accumulation of species of Darwin's finches with time, back-calculated from the estimated ages (in millions of years, or MY) of contemporary species in the absence of known extinctions. The accumu- lation of species parallels the accumulation of islands with time, as de- termined from estimations of island age and elevation in relation to sea ns for speciation to occur and level. More islands provide more condi ‘species to persist. From Grant (2001). that the islands have always been much as they are today in terms of geography, climate, and vegetation. If this is correct, the finches’ adaptive radiation can be viewed as a process of differentiation that results in the occupancy of all ecological niches present at the outset—rather like filling empty boxes, ‘one species per box. Indeed, this is how early writers on the subject viewed the radiation of the finches, stressing the absence or scarcity of competitors in the boxes asa facilitat- ing factor (Huxley 1942, Simpson 1944, Lack 1947, Grant 1999). In the modern version, the boxes are replaced by adap- tive peaks in a more or less fixed landscape. This view implies that diversification is rapid early in the radiation and then slows down as ecological opportunities diminish. Some radiations of other organisms elsewhere conform to this pattern (Schluter 2000). However, taken at face value, the phylogeny of Darwin's finches shows exactly the opposite pattern: a slow start followed by recent, rapid diversification (figure 7). The species occupy adaptive peaks, but the fixity of the ecological landscape that allowed them to do so is questionable. In fact, the islands and their inhabitants have changed radically. Three million years ago, there were far fewer islands than today, perhaps only five (Grant and Grant 1998), ‘The number of islands increased as a result of voleanic activity centered on and near a hotspot beneath the western island of Fernandina, Climate changed as well. The average air 972. BioScience + October 2003 / Vol. 53 No. 10 temperature declined but, more important than this, the world’s climate underwent a sharp transi- tion 2.75 million years ago with the abrupt onset of glaciation (Cane and Molnar 2001). In the last million years the climate has oscillated between glacial and interglacial conditions at about 100,000 year intervals. Global fluctuations in climate were experienced locally, in the Galipagos and elsewhere in tropical America. This has been revealed by the isotopic oxygen signatures of temperature in Andean ice cores (Seltzer et al. 2002), by coral cores in Galapagos (Dunbar et al. 1994), and by pollen cores in Galpagos (Colinvaux 1972, 1984) and in continental South and Central American lakes (Bush et al. 1992) Most of the contemporary finches evolved in the last million years, soit is important to know ‘what happened during these cycles. The two major effects of glacial-interglacial cycles were the de- pression of temperatures and of sea level relative to contemporary levels. The last Ice Age cooling resulted in a drop of 3°C to 4°C in the equatorial Pacific, reaching a minimum about 21,000 years ago (Kerr 2001). The previous deglacia~ tion, about 130,000 years ago, was associated with a drop of 2°C to 6°C (Tudhope etal. 2001).Sea level fell with the temperature. The decline was gradual from the current level (about 120,000 years ago) to about 60 meters (m) lower (about 30,000 years ago); then an abrupt further decrease occurred to about 125 m below the current level (Lambeck and Chappell 2001). As a consequence, islands were larger and distances between them were shorter. Thus, both temperature and sea level were usually lower and never much higher than they are today. ‘The food of finches—plants and arthropods, the latter feeding on the plants and on each other—must have been affected by these geophysical and climatic changes. First, new species of plants and arthropods would have arrived by immigration. We do not know when this happened or which species were involved. For Galapagos, unlike Hawaii (eg, Givnish 1998, Wright etal. 2000), there are no molecular phylogenies of plants to help in reconstructing paleofloras, and the phylogenies of insects are too scarce to be useful (Finston and Peck 1997, Sequeira et al. 2000). That situation needs to be rectified. Second, other species, perhaps influenced by the immigrants, would have become extinct. Severe and extensive droughts would have been particularly crucial and cruel times for many “organisms, including finches. Third, the temperature- and moisture-dependent altitudinal zonation of plants would have shifted upward and downward at different times; hence, the highest and lowest habitats would have been most vulnerable to elimination, as noted elsewhere (Prodon et al, 2002). Plant distributions would have changed across the archipelago. Islands Speciesea ‘The evidence of a change in the upland forests isthe rel- ative scarcity of endemic plants (Johnson and Raven 1973). ‘The evidence of a change in the lowest zone is the anomalous ‘occurrence of plants on some islands with apparently un- suitable climates and soil. For example, the tree Erythrina velu- tina occurs at mid elevations on the high islands of Santa Cruz, Santiago, and Isabela. A single tree of this species occurs on the low arid island of Genovesa, and fewer than a dozen oc- cur on the low, arid, and even more remote island of Wolf. ‘Similarly, a few Zanthaxylum fagara trees on Santa Cruz and San Cristobal occur close to the coast. These may be the remnants of much larger populations on these islands under cooler, wetter, or less seasonally arid conditions than those that prevail today. Temperatures and precipitation changed markedly from one state to another long enough (> 1000 years; Colinvaux 1972, Riedinger et al. 2002) for vegeta zones to shift (Woodward 1987). On some occasions, how- ever, significant changes in temperature occurred in as short a time as a hundred years, perhaps less (Bush et al. 1992), Large, abrupt, and widespread climate changes with major consequences for the biota have occurred repeatedly in the past, when the Earth system was forced across thresholds (Alley et al. 2003). ‘The macroevolutionary pattern and the buildup of complex communities from simple ones In view of the strong environmental changes in the archi- pelago, itis scarcely likely that all current ecological niches were available when the finches’ ancestors arrived. Rather, the numbers and types of opportunities for finch evolution incteased as the number of islands increased and the climate and vegetation changed. According to this view, the adaptive radiation and the buildup of species-rich commu- nities were largely molded by environmental change; the particular species originated when they did, and no earlier, in response to particular environments prevailing then, When the first finches arrived on Galapagos, they may have encountered a climate and vegetation more like those of modern-day Cocos Island: warmer, wetter, and more humid conditions, fostering rain forest from the coast to the island peaks (Grant 1999, Grant and Grant 2002b). Cocos Island has temperatures similar to those of the coastal habitats in the Galépagos and rainfall equivalent to what the Galapagos now receives in an El Nifo year at high elevations. Reason- ing from the evidence of modern finches, we suggest the ini tial evolutionary pathway taken by the finches was toward the exploitation of small arthropods, and of nectar and pollen from small flowers, ina rain forest-like environment. ‘The radiation began when the inital species spit into two lineages of Certhidea warbler finches (figure 8) after the ini- tial pathway had been taken. One group of populations (Certhidea olivacea) inhabits moist upland forest, and the other group (Certhidea fusca) occupies lower habitats on other, mainly low, islands. Remarkably, despite their long separation, the two groups have retained similar mate recog- nition systems, and for that reason we refer to them as lineages Plenary Figure 8, Reconstruction of finch phylogeny based on ‘microsatellite DNA. Horizontal branch lengths are pro- portional to units of genetic distance (G,,) as indicated by the scale. Numbers refer to percentage bootstrap support for the nodes by two methods. Mean weights are given on the right, together with symbols of male plumay black, partially black, or brown or green. Alternative reconstructions that use morphology, allozymes, or mito- chondrial DNA are similar, differing in relatively small details. Species, from top to bottom: Geospiza fuliginosa, Geospiza fortis, Geospiza magnirostris, Geospiza scandens, Geospiza conirostris, Geospiza diffcilis, Camarhynchus parvulus, Camarhynchus psittacula, Camarhynchus pauper, Camarhynchus pallida, Platyspiza crassirostrs, Certhidea fusca, Pinaroloxias inornata, and Certhidea olivacea. From Petren and colleagues (1999). October 2003 / Vol. 53 No. 10 + BioScience 973Plenum and not species (Grant and Grant 2002b). Another remark- able feature is that they have remained relatively undifferen- tiated in morphology, ecology, and behavior. This is not ‘expected on the basis ofthe view that niches were varied, plen- tiful, and evolutionarily within reach at that time. However we must acknowledge the possibility, perhaps even the prob- ability that extinction has robbed us of other species that were formed then. The morphological similarity of these finches, contrasting with their distinctness from continental rela- tives, argues for an early adaptation to an unusual niche, One of the warbler finch lineages gave rise to all other finch species. Early products ofthe diversification were the veg etarian finch (Platyspiza crassirastris), the Cocos finch (Pinarolaxias inornata) on either Galipagos or Cocos Island (Grant and Grant 2002b), and the sharp-beaked ground finch (G. dffclis). The most recent products were a group of ‘ground finch species (Geaspiza) and a group of tree finch species (Camarhynchus and Cactospiza) (figure 8). Effects of environmental change have left a different hi torical imprint on the older species. Populations of G. difi- cilis dlfer strongly in morphology and ecology toa degree un- matched by all other, and younger, species in the genus Geospiza and by the warbler finches that preceded them. Some G. dffcilis have persisted in Zanthaxylum forest at mid and upper elevations, which we believe to be old, and others have entered arid lowland habitat, pethaps when the Zanthoxylum forest gradually disappeared from low islands as the climate changed. This may have been the first step of the radiation of ground finches. In contrast to the G. difcilis populations, populations of the vegetarian finch are mor- pphologically and ecologically very similar. Limited genetic data (Petren et al. 1999) suggest that they separated from each other recently. This is surprising, as it isnot expected from the age of the species or from the presumed stability of its mid- elevation transition zone habitat. The vegetarian finch may have become restricted to one or two islands, and other pop- ulations or even related species may have become extinct, in response to one of the recent extreme fluctuations in climate. Its vegetarian diet may have made it vulnerable in times of drought, and competition with other species may have been an additional factor ‘The importance of environmental change in speciation is, further suggested by the fact that in the last million years new species evolved in the habitats most vulnerable to change: Geospiea were added to lowland habitats, and Camarhynchus were added to the upland humid forest. The change in climate toward seasonal aridity and the development of arid lowland habitat provided the opportunity for a new, granivorous way of finch life, now adopted by Geospiza species. Some of these modern species may have contributed to the extinction of older ones through competitive superiority in a changing environment. This is one possible interpretation of the contrast between the morphological distinctness ofthe three older groups, Certhidea, Platyspiza, and G. diffcilis, and the morphological similarity of species in the younger genera, Camarhynchus, Cactospiza, and Geospiza. 974 BioScience + October 2003 / Vol. 53 No. 10 “These ideas on speciation and extinction, together with ob- servations of the colonization of Daphne Major by G. magni- rostris (Grant et al. 2001), suggest that periods of expansion such as the one in progress are preceded and followed by periods of range contraction and extinction caused by envi- ronmental change. Distributions of habitats, sea level, island and population sizes, and degrees of isolation provide favorable conditions for divergence of small populations in isolation at some times and for dispersal, mixing, establish- ‘ment of sympatry, and hybridization at others. The buildup of complex communities from simple ones isnot smooth, con- tinuous, and regular, but a process of gains and losses with a net accumulation of species over the long term. Conclusions According to the standard allopatric model, speciation begins with the establishment of a new population, continues with the divergence of that population from its parent population, and is completed when members of two diverged populations can coexist in sympatry without interbreeding. We stand a virtually negligible chance of observing the whole process under natural circumstances. Nevertheless it is possible to make relevant observations in nature of all steps in the process. We have described the strong role played by envi- ronmental change at each ofthe three steps in the speciation of Darwin's finches. The full adaptive radiation was pro- duced by a repetition of these steps, each with a different product under somewhat different circumstances. The challenge now is to account forthe differences in terms of past environments, without the help of fossils of finches or of ‘other members of the biota. We have sketched a framework for doing this by using molecular genetic information to «estimate the finch phylogeny and using geological and climatic information to reconstruct Galdpagos environments in the past 2 million to 3 million years. A better understanding of ‘environmental change on this time scale will help to explain why 14 species were formed, what their sequence of origin was, and why they evolved their particular unique features. There may be more history to uncover in finch DNA, if only we can work out how to read it. Acknowledgments: We thank Ken Petren for figure 8 and Phil Hedrick, Fritz ‘Trillmich, and an anonymous reviewer for comments on the ‘manuscript. 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