Evolution can be predicted in the short term from a knowledge of selection and inheritance. However, in the long term evolution is unpredictable because environments, which determine the directions and magnitudes of selection coefficients, fluctuate unpredictably. These two features of evolution, the predictable and unpredictable, are demonstrated in a study of two populations of Darwin's finches on the Galápagos island of Daphne Major. From 1972 to 2001, Geospiza fortis (medium ground finch) and Geospiza scandens (cactus finch) changed several times in body size and two beak traits. Natural selection occurred frequently in both species and varied from unidirectional to oscillating, episodic to gradual. Hybridization occurred repeatedly though rarely, resulting in elevated phenotypic variances in G. scandens and a change in beak shape. The phenotypic states of both species at the end of the 30-year study could not have been predicted at the beginning. Continuous, long-term studies are needed to detect and interpret rare but important events and nonuniform evolutionary change.
Darwin's finches, inhabiting the Galápagos archipelago and Cocos Island, constitute an iconic model for studies of speciation and adaptive evolution. Here we report the results of whole-genome re-sequencing of 120 individuals representing all of the Darwin's finch species and two close relatives. Phylogenetic analysis reveals important discrepancies with the phenotype-based taxonomy. We find extensive evidence for interspecific gene flow throughout the radiation. Hybridization has given rise to species of mixed ancestry. A 240 kilobase haplotype encompassing the ALX1 gene that encodes a transcription factor affecting craniofacial development is strongly associated with beak shape diversity across Darwin's finch species as well as within the medium ground finch (Geospiza fortis), a species that has undergone rapid evolution of beak shape in response to environmental changes. The ALX1 haplotype has contributed to diversification of beak shapes among the Darwin's finches and, thereby, to an expanded utilization of food resources.
Competitor species can have evolutionary effects on each other that result in ecological character displacement; that is, divergence in resource-exploiting traits such as jaws and beaks. Nevertheless, the process of character displacement occurring in nature, from the initial encounter of competitors to the evolutionary change in one or more of them, has not previously been investigated. Here we report that a Darwin's finch species (Geospiza fortis) on an undisturbed Galá pagos island diverged in beak size from a competitor species (G. magnirostris) 22 years after the competitor's arrival, when they jointly and severely depleted the food supply. The observed evolutionary response to natural selection was the strongest recorded in 33 years of study, and close to the value predicted from the high heritability of beak size. These findings support the role of competition in models of community assembly, speciation, and adaptive radiations.
Darwin's finches are a classic example of species diversification by natural selection. Their impressive variation in beak morphology is associated with the exploitation of a variety of ecological niches, but its developmental basis is unknown. We performed a comparative analysis of expression patterns of various growth factors in species comprising the genus Geospiza. We found that expression of Bmp4 in the mesenchyme of the upper beaks strongly correlated with deep and broad beak morphology. When misexpressed in chicken embryos, Bmp4 caused morphological transformations paralleling the beak morphology of the large ground finch G. magnirostris.
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 Darwin's finch populations on a Galápagos 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.
A classic textbook example of adaptive radiation under natural selection is the evolution of 14 closely related species of Darwin's finches (Fringillidae, Passeriformes), whose primary diversity lies in the size and shape of their beaks. Thus, ground finches have deep and wide beaks, cactus finches have long and pointed beaks (low depth and narrower width), and warbler finches have slender and pointed beaks, reflecting differences in their respective diets. Previous work has shown that even small differences in any of the three major dimensions (depth, width and length) of the beak have major consequences for the overall fitness of the birds. Recently we used a candidate gene approach to explain one pathway involved in Darwin's finch beak morphogenesis. However, this type of analysis is limited to molecules with a known association with craniofacial and/or skeletogenic development. Here we use a less constrained, complementary DNA microarray analysis of the transcripts expressed in the beak primordia to find previously unknown genes and pathways whose expression correlates with specific beak morphologies. We show that calmodulin (CaM), a molecule involved in mediating Ca2+ signalling, is expressed at higher levels in the long and pointed beaks of cactus finches than in more robust beak types of other species. We validated this observation with in situ hybridizations. When this upregulation of the CaM-dependent pathway is artificially replicated in the chick frontonasal prominence, it causes an elongation of the upper beak, recapitulating the beak morphology of the cactus finches. Our results indicate that local upregulation of the CaM-dependent pathway is likely to have been a component of the evolution of Darwin's finch species with elongated beak morphology and provide a mechanistic explanation for the independence of beak evolution along different axes. More generally, our results implicate the CaM-dependent pathway in the developmental regulation of craniofacial skeletal structures.
Homoploid hybrid speciation in animals has been inferred frequently from patterns of variation, but few examples have withstood critical scrutiny. Here we report a directly documented example, from its origin to reproductive isolation. An immigrant Darwin's finch to Daphne Major in the Galápagos archipelago initiated a new genetic lineage by breeding with a resident finch (). Genome sequencing of the immigrant identified it as a male that originated on Española>100 kilometers from Daphne Major. From the second generation onward, the lineage bred endogamously and, despite intense inbreeding, was ecologically successful and showed transgressive segregation of bill morphology. This example shows that reproductive isolation, which typically develops over hundreds of generations, can be established in only three.
Microevolution of quantitative traits in the wild can be predicted from a knowledge of selection and genetic parameters. Testing the predictions requires measurement of the offspring of the selected group, a requirement that is difficult to meet. We present the results of a study of Darwin's finches on the Galápagos island of Daphne Major where this requirement is met. The study demonstrates microevolutionary consequences of natural selection.
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