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      Evolution of Darwin's finches and their beaks revealed by genome sequencing.

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          Abstract

          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.

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          Testing for ancient admixture between closely related populations.

          Eric Durand, Nick Patterson, David Reich … (2011)
          One enduring question in evolutionary biology is the extent of archaic admixture in the genomes of present-day populations. In this paper, we present a test for ancient admixture that exploits the asymmetry in the frequencies of the two nonconcordant gene trees in a three-population tree. This test was first applied to detect interbreeding between Neandertals and modern humans. We derive the analytic expectation of a test statistic, called the D statistic, which is sensitive to asymmetry under alternative demographic scenarios. We show that the D statistic is insensitive to some demographic assumptions such as ancestral population sizes and requires only the assumption that the ancestral populations were randomly mating. An important aspect of D statistics is that they can be used to detect archaic admixture even when no archaic sample is available. We explore the effect of sequencing error on the false-positive rate of the test for admixture, and we show how to estimate the proportion of archaic ancestry in the genomes of present-day populations. We also investigate a model of subdivision in ancestral populations that can result in D statistics that indicate recent admixture.
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            Bmp4 and morphological variation of beaks in Darwin's finches.

            Arhat Abzhanov, Meredith E Protas, B Grant … (2004)
            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.
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              The calmodulin pathway and evolution of elongated beak morphology in Darwin's finches.

              P. Grant, Christine Hartmann, Kevin Kuo … (2006)
              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.
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                Author and article information

                Journal
                Journal ID (iso-abbrev): Nature
                Title: Nature
                ISSN (Electronic): 1476-4687
                ISSN (Print): 0028-0836
                Publication date (Electronic): Feb 19 2015
                Volume: 518
                Issue: 7539
                Affiliations
                [1 ] Department of Medical Biochemistry and Microbiology, Uppsala University, SE-751 23 Uppsala, Sweden.
                [2 ] Department of Animal Breeding and Genetics, Swedish University of Agricultural Sciences, SE-75007 Uppsala, Sweden.
                [3 ] 1] Department of Medical Biochemistry and Microbiology, Uppsala University, SE-751 23 Uppsala, Sweden [2] Department of Plant Physiology, Umeå University, SE-901 87 Umeå, Sweden.
                [4 ] Department of Ecology and Evolutionary Biology, Princeton University, Princeton, New Jersey 08544, USA.
                [5 ] 1] Department of Medical Biochemistry and Microbiology, Uppsala University, SE-751 23 Uppsala, Sweden [2] Department of Animal Breeding and Genetics, Swedish University of Agricultural Sciences, SE-75007 Uppsala, Sweden [3] Department of Veterinary Integrative Biosciences, Texas A&M University, College Station, Texas 77843-4458, USA.
                Article
                Publisher Item ID: nature14181
                DOI: 10.1038/nature14181
                PubMed ID: 25686609
                SO-VID: f823df29-9b63-48aa-9173-4a6214dd53b1
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