B. R. Grant

Hybridization of Bird Species

Hybridization, the interbreeding of species, provides favorable conditions for major and rapid evolution to occur. In birds it is widespread. Approximately one in ten species is known to hybridize, and the true global incidence is likely to be much higher. A longitudinal study of Darwins finch populations on a Gal�pagos island shows that hybrids exhibit higher fitness than the parental species over several years. Hybrids may be at an occasional disadvantage for ecological rather than genetic reasons in this climatically fluctuating environment. Hybridization presents challenges to the reconstruction of phylogenies, formulation of biological species concepts and definitions, and the practice of biological conservation.

Evolution of Darwin’s finches caused by a rare climatic event

Populations of animals and plants often undergo conspicuous ecological changes when subjected to climatic extremes. Evolutionary changes may accompany them but are less easily detected. We show that Darwin’s finches on a Galapagos island underwent two evolutionary changes after a severe El Nino event caused changes in their food supply. Small beak sizes were selectively favoured in one granivorous species when large seeds became scarce. The effects of selection were transmitted to the next generation as a result of high trait heritabilities. Hybridization between this species and two others resulted in gene exchange, but only after the El Nino when hybrid fitness was much enhanced under the altered feeding conditions. These observations imply that if global warming increases the frequency or severity of El Nino events on the Galapagos, microevolutionary changes in animal and plant populations are to be anticipated.

A PHYLOGENY OF DARWIN'S FINCHES BASED ON MICROSATELLITE DNA LENGTH VARIATION

Allele length variation at 16 microsatellite loci was used to estimate the phylogeny of 13 out of the 14 species of Darwins finches. The resulting topology was similar to previous phylogenies based on morphological and allozyme variation. An unexpected result was that genetic divergence among Galápagos Island populations of the warbler finch (Certhidea olivacea) predates the radiation of all other Darwins finches. This deep split is surprising in view of the relatively weak morphological differentiation among Certhidea populations and supports the hypothesis that the ancestor of all Darwins finches was phenotypically similar to Certhidea. The results also resolve a biogeographical problem: the Cocos Island finch evolved after the Galápagos finch radiation was under way, supporting the hypothesis that this distant island was colonized from the Galápagos Islands. Monophyletic relationships are supported for both major groups, the ground finches (Geospiza) and the tree finches (Camarhynchus and Cactospiza), although the vegetarian finch (Platyspiza crassirostris) appears to have diverged prior to the separation of ground and tree finches. These results demonstrate the use of microsatellites for reconstructing phylogenies of closely related species and interpreting their evolutionary and biogeographic histories.

Comparative landscape genetics and the adaptive radiation of Darwin's finches: the role of peripheral isolation.

We use genetic divergence at 16 microsatellite loci to investigate how geographical features of the Galápagos landscape structure island populations of Darwins finches. We compare the three most genetically divergent groups of Darwins finches comprising morphologically and ecologically similar allopatric populations: the cactus finches (Geospiza scandens and Geospiza conirostris), the sharp‐beaked ground finches (Geospiza difficilis) and the warbler finches (Certhidea olivacea and Certhidea fusca). Evidence of reduced genetic diversity due to drift was limited to warbler finches on small, peripheral islands. Evidence of low levels of recent interisland migration was widespread throughout all three groups. The hypothesis of distance‐limited dispersal received the strongest support in cactus and sharp‐beaked ground finches as evidenced by patterns of isolation by distance, while warbler finches showed a weaker relationship. Support for the hypothesis that gene flow constrains morphological divergence was only found in one of eight comparisons within these groups. Among warbler finches, genetic divergence was relatively high while phenotypic divergence was low, implicating stabilizing selection rather than constraint due to gene flow. We conclude that the adaptive radiation of Darwins finches has occurred in the presence of ongoing but low levels of gene flow caused by distance‐dependent interisland dispersal. Gene flow does not constrain phenotypic divergence, but may augment genetic variation and facilitate evolution due to natural selection. Both microsatellites and mtDNA agree in that subsets of peripheral populations of two older groups are genetically more similar to other species that underwent dramatic morphological change. The apparent decoupling of morphological and molecular evolution may be accounted for by a modification of Lacks two‐stage model of speciation: relative ecological stasis in allopatry followed by secondary contact, ecological interactions and asymmetric phenotypic divergence.

Seasonal Variation in Feeding Habits of Darwin's Ground Finches

We investigated the effects of seasonal variation in food abundance on food partitioning among Darwins ground finches of the genus Geospiza. Finch populations, the availability of seed of fruits, and finch feeding habits were measured during 2 visits to each of 4 study sites on 3 Galapagos islands. Our 1st visit was made near the end of the 1973 rains at a time of seasonal food abundance and the 2nd, 6—8 mo later, when food was scarce. If interspecific competition prevails, finch populations should decline from wet to dry season in response to declining food availability. At 2 sites where food supplies declined sharply, so did an index of finch numbers; at the other 2 sites, both food supplies and finch numbers remained high. Total finch biomass at 5 dry—season study sites was correlated with food abundance but was not at 8 wet—season study sites. If interspecific competition is stronger, diets of finch species should diverge as food becomes scarce, but if intraspecific competition is stronger, diets should expand and overlap among species increase. At all 4 sites, finch species diverged in their diets and took a narrower range of foods in the dry season. All species shifted from a common wet—season diet of soft, easy—to—handle seeds and fruits to different diets reflecting the morphological specializations of each species. The results are consistent with interspecific competition for food occuring at all sides, but other explanations cannot be ruled out. Even where food remained relatively abundant, species diets changed and overlapped less. Intense competition was not, therefore, a necessary condition for seasonal diet changes; these may have been simple proximate responses to food availability. Existing foraging theory does not predict these results or others, because the assumption that available foods do not change qualitatively between seasons is violated. Where food greatly decreased, inter— and intraspecific competition may have caused the death or dispersal of most of the finches in the wet—season populations and diet divergence minimized interspecific competition are probably complemented by year—to—year differences caused by the unpredictable Galapagos rainfall.

Two developmental modules establish 3D beak-shape variation in Darwin's finches

Bird beaks display tremendous variation in shape and size, which is closely associated with the exploitation of multiple ecological niches and likely played a key role in the diversification of thousands of avian species. Previous studies have demonstrated some of the molecular mechanisms that regulate morphogenesis of the prenasal cartilage, which forms the initial beak skeleton. However, much of the beak diversity in birds depends on variation in the premaxillary bone. It forms later in development and becomes the most prominent functional and structural component of the adult upper beak/jaw, yet its regulation is unknown. Here, we studied a group of Darwins finch species with different beak shapes. We found that TGFβIIr, β-catenin, and Dickkopf-3, the top candidate genes from a cDNA microarray screen, are differentially expressed in the developing premaxillary bone of embryos of species with different beak shapes. Furthermore, our functional experiments demonstrate that these molecules form a regulatory network governing the morphology of the premaxillary bone, which differs from the network controlling the prenasal cartilage, but has the same species-specific domains of expression. These results offer potential mechanisms that may explain how the tightly coupled depth and width dimensions can evolve independently. The two-module program of development involving independent regulating molecules offers unique insights into how different developmental pathways may be modified and combined to induce multidimensional shifts in beak morphology. Similar modularity in development may characterize complex traits in other organisms to a greater extent than is currently appreciated.

Natural Selection in a Population of Darwin's Finches

An exceptionally wet year followed by two very dry years severely perturbed the food supply of cactus finches (Geospiza conirostris) on Isla Genovesa, Galapagos. This provided us with a natural experiment for detecting and interpreting selection acting on bill shape in response to the near elimination of some of the food items and availability of others. Long-billed birds had a survival disadvantage associated with the absence of Opuntia flowers and fruits, which they normally exploit. This selection event was followed by another favoring birds with deep beaks capable of extracting the only available food, arthropods from beneath the bark of trees and within Opuntia trunks and old pads. For young birds, the ability to develop (learn) techniques for extracting a new food item was a better predictor of survival than was bill shape. Among the group that acquired these skills, more of the birds with deep bills survived, as was the case for the adults. During 1984, males that obtained females had deeper bills than those that failed to do so. Because this mating advantage did not occur in years without natural selection, we suggest that birds with deep bills had more energy available for courtship. Using the same approach, we also describe a parallel case of natural selection in a sympatric congener, G. magnirostris, in which birds with deep beaks capable of cracking large and hard Cordia lutea seeds were favored. The population has undergone little or no evolutionary change in bill dimensions in response to selection during the last nine years, despite the presence of high levels of additive genetic variance. Evolutionary change has not occurred because the action of selection on one trait in one direction has been counteracted by selection in the opposite direction on another, positively correlated trait. Changes in the proportions of dry-season niches among years cause changes in the proportions of birds with certain beak morphologies and feeding skills best suited to exploiting them. Therefore, the population tracks a moving peak in an adaptive landscape under environmental fluctuations, and there is more than one individual fitness optimum within the range of phenotypes in the population.

Neutral locus heterozygosity, inbreeding, and survival in Darwin's ground finches (Geospiza fortis and G. scandens).

Comprehensive long-term studies of isolated populations provide valuable comparative data that may be used to evaluate different methods for quantifying the relationship between genetic diversity and fitness. Here, we report on data collected from large and well-characterized cohorts of the two numerically dominant species of Darwins finches on Isla Daphne Major, Galápagos, Ecuador – Geospiza fortis and G. scandens. Multilocus microsatellite (SSR) genetic diversity estimates (heterozygosity and [dmacr ]2) and pedigree-based estimates of the inbreeding coefficient (f) were compared to each other and to two fitness components: lifespan and recruitment. In the larger sample of G. fortis, heterozygosity (H) was correlated with both fitness components, but no relationship was detected in the smaller sample of G. scandens. Analyses of the inbreeding coefficient detected highly significant relationships between f and recruitment, but no relationship between f and overall lifespan. The [dmacr ]2 statistic showed no relationship to either fitness component. When the two SSR-based estimators were compared to f, [dmacr ]2 was correlated with f in G. fortis in the predicted direction, while in G. scandens the relationship was positive. Multilocus heterozygosity was correlated with f in G. fortis but not in the G. scandens sample. A pedigree simulation demonstrated that the variation in true autozygosity can be large among individuals with the same level of inbreeding. This observation may supplement the interpretation of patterns relevant to the local (locus-specific) and general (genome-wide) effects hypotheses, which have been proposed to explain the mechanism responsible for associations between genetic diversity and fitness.

NICHE SHIFTS AND COMPETITION IN DARWIN'S FINCHES: GEOSPIZA CONIROSTRIS AND CONGENERS

The idea that interspecific competition is an important process in structuring communities stems largely from David Lacks work with Darwins Finches (Lack, 1940, 1945, 1947, 1969). Lack made ecological inferences about feeding niches from analyses of bill sizes and shapes. He listed several instances where the niches of coexisting species were different, and where the niche of an absent species appeared to be occupied by one or more species present. These examples he interpreted as evidence of competitive displacement and exclusion. Lacks aim was to offer a coherent theoretical framework for understanding the adaptive radiation of Darwins Finches, not to test specific hypotheses. In contrast, our aim is to test the hypothesis of interspecific competition. This is needed because the evidence in general for interspecific competition as an important factor in determining niche relationships and community patterns has been critically debated recently (e.g., Connell, 1975, 1978, 1980; Wiens, 1977; Connor and Simberloff, 1978, 1979; Simberloff, 1978; Strong et al., 1979; Abbott, 1980; Grant and Abbott, 1980; Ricklefs and Travis, 1980; Rotenberry and Wiens, 1980; Wiens and Rotenberry, 1980). We can return to Darwins Finches to perform such tests without circularity by obtaining and applying quanRevised October 20, 1981

Insights into the evolution of Darwin’s finches from comparative analysis of the Geospiza magnirostris genome sequence

BackgroundA classical example of repeated speciation coupled with ecological diversification is the evolution of 14 closely related species of Darwin’s (Galápagos) finches (Thraupidae, Passeriformes). Their adaptive radiation in the Galápagos archipelago took place in the last 2–3 million years and some of the molecular mechanisms that led to their diversification are now being elucidated. Here we report evolutionary analyses of genome of the large ground finch, Geospiza magnirostris.Results13,291 protein-coding genes were predicted from a 991.0 Mb G. magnirostris genome assembly. We then defined gene orthology relationships and constructed whole genome alignments between the G. magnirostris and other vertebrate genomes. We estimate that 15% of genomic sequence is functionally constrained between G. magnirostris and zebra finch. Genic evolutionary rate comparisons indicate that similar selective pressures acted along the G. magnirostris and zebra finch lineages suggesting that historical effective population size values have been similar in both lineages. 21 otherwise highly conserved genes were identified that each show evidence for positive selection on amino acid changes in the Darwins finch lineage. Two of these genes (Igf2r and Pou1f1) have been implicated in beak morphology changes in Darwin’s finches. Five of 47 genes showing evidence of positive selection in early passerine evolution have cilia related functions, and may be examples of adaptively evolving reproductive proteins.ConclusionsThese results provide insights into past evolutionary processes that have shaped G. magnirostris genes and its genome, and provide the necessary foundation upon which to build population genomics resources that will shed light on more contemporaneous adaptive and non-adaptive processes that have contributed to the evolution of the Darwin’s finches.