[Show abstract][Hide abstract] ABSTRACT: We recently used genome sequencing to study the evolutionary history of the Darwin's finches. A prominent feature of our data was that different polymorphic sites in the genome tended to indicate different genetic relationships among these closely related species. Such patterns are expected in recently diverged genomes as a result of incomplete lineage sorting. However, we uncovered conclusive evidence that these patterns have also been influenced by interspecies hybridisation, a process that has likely played an important role in the radiation of Darwin's finches. A major discovery was that segregation of two haplotypes at the ALX1 locus underlies variation in beak shape among the Darwin's finches, and that differences between the two haplotypes in a 240 kb region in blunt and pointed beaked birds involve both coding and regulatory changes. As we review herein, the evolution of such adaptive haplotypes comprising multiple causal changes appears to be an important mechanism contributing to the evolution of biodiversity.
[Show abstract][Hide abstract] ABSTRACT: The recent trend for journals to require open access to primary data included in publications has been embraced by many biologists, but has caused apprehension amongst researchers engaged in long-term ecological and evolutionary studies. A worldwide survey of 73 principal investigators (Pls) with long-term studies revealed positive attitudes towards sharing data with the agreement or involvement of the PI, and 93% of PIs have historically shared data. Only 8% were in favor of uncontrolled, open access to primary data while 63% expressed serious concern. We present here their viewpoint on an issue that can have non-trivial scientific consequences. We discuss potential costs of public data archiving and provide possible solutions to meet the needs of journals and researchers.
Full-text · Article · Oct 2015 · Trends in Ecology & Evolution
[Show abstract][Hide abstract] ABSTRACT: Darwin's finches, inhabiting the Galápagos archipelago and Cocos Island, constitute an iconic model for studies of speci-ation 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. Hybrid-ization 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.
[Show abstract][Hide abstract] ABSTRACT: Abstract This article explores how introgressive hybridization enhances the evolutionary effects of natural selection and how, reciprocally, natural selection can enhance the evolutionary effects of introgression. Both types of interaction were observed during a 40-year study of Darwin's finches (Geospiza) on the small Galápagos island of Daphne Major. Hybrids, produced rarely by Geospiza fortis (medium ground finch) breeding with Geospiza scandens (cactus finch) and Geospiza fuliginosa (small ground finch), survived and bred as well as the parental species in the past 3 decades. By backcrossing, they increased the standing genetic variation and thereby the evolutionary responsiveness of the populations to natural selection. Natural selection occurred in droughts and oscillated in direction as a result of climatically induced fluctuations in food composition. Introgressive hybridization has led to the formation of a new lineage. It was initiated by a large, introgressed, hybrid male with a unique song and genetic marker that immigrated from the nearby island of Santa Cruz and bred with local hybrids and with G. fortis. All members of the lineage died in the 2003-2005 drought except a brother and a sister, who then bred with each other. Subsequent increase in the lineage was facilitated by selective mortality of the largest G. fortis. Breeding endogamously, the lineage is behaving as a biological species.
No preview · Article · May 2014 · The American Naturalist
[Show abstract][Hide abstract] ABSTRACT: Hybridization can cause two species to fuse into a single population. New observations suggest that two species of Darwin's finches are hybridizing on a Galapagos island, and that a third one has disappeared through interbreeding.
[Show abstract][Hide abstract] ABSTRACT: Introgression of genes through hybridization has been proposed to be an important driver of speciation, but in animals this has been shown only in relatively few cases until recently. Additionally, introgressive hybridization among non-sister species leads to a change in the gene tree topology of the concerned loci and thus complicates phylogenetic reconstruction. However, such cases of ancient introgression have been very difficult to demonstrate in birds. Here, we present such an example in an island bird subspecies, the Genovesa mockingbird (Mimus parvulus bauri). We assessed phylogenetic relationships and population structure among mockingbirds of the Galápagos archipelago using mitochondrial and nuclear DNA sequences, autosomal microsatellites, and morphological measurements. Mitochondrial haplotypes of Genovesa mockingbirds clustered closely with the haplotypes from two different species, San Cristóbal (M. melanotis) and Española (M. macdonaldi) mockingbirds. The same pattern was found for some haplotypes of two nuclear gene introns, while the majority of nuclear haplotypes of Genovesa mockingbirds were shared with other populations of the same species (M. parvulus). At 26 autosomal microsatellites, Genovesa mockingbirds grouped with other M. parvulus populations. This pattern shows that Genovesa mockingbirds contain mitochondria and some autosomal alleles that have most likely introgressed from M. melanotis into a largely M. parvulus background, making Genovesa mockingbirds a lineage of mixed ancestry, possibly undergoing speciation. Consistent with this hypothesis, mockingbirds on Genovesa are more clearly differentiated morphologically from other M. parvulus populations than M. melanotis is from M. parvulus.
No preview · Article · Jul 2013 · Molecular Phylogenetics and Evolution
[Show abstract][Hide abstract] ABSTRACT: A 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.
13,291 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 Darwin's 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.
These 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.
[Show abstract][Hide abstract] ABSTRACT: Events occurring at the founding of a population, and in the next few generations, are potentially of great importance for
the future evolution of the population. This study reports demographic, genetic, and morphological changes that took place
during and after the colonization of the small Galápagos island of Daphne Major by three male and two female large ground
finches, Geospiza magnirostris, at the end of 1982. Using assignment tests with microsatellite DNA data we demonstrate heterogeneity among the immigrants.
Their sources included both a near island (Santa Cruz) and a far island (Marchena). However, almost all immigrants that stayed
to breed were from an intermediate island (Santiago) and its satellites. Song may have been responsible for this selectivity.
Mean heterozygosity stayed roughly constant over the next 15 years while allelic diversity almost doubled, after an initial
decline, as the breeding population increased to a maximum of 30 pairs. Although close inbreeding occurred, with a reduction
in heterozygosity, an expected net decline in heterozygosity did not occur, for two reasons: it was counteracted by continuing
gene flow from immigrants at a low rate, and inbred birds (in one cohort) were at a selective disadvantage. An abrupt step-function
shift in beak shape occurred after 9 years. Thus the study provides evidence of drift and selection causing morphological
and genetic divergence in the establishment of a new population and in the first few generations.
Key wordsbeak shape–cultural and genetic drift–founders–heterozygosity–inbreeding–island colonization–microsatellites–natural selection
[Show abstract][Hide abstract] ABSTRACT: The study describes >400 major histocompatibility complex (MHC) class II B exon 2 and 114 intron 2 sequences of 36 passerine bird species, 13 of which belong to the group of Darwin's finches (DFs) and the remaining 23 to close or more distant relatives of DFs in Central and South America. The data set is analyzed by a combination of judiciously selected statistical methods. The analysis reveals that reliable information concerning MHC organization, including the assignment of sequences to loci, and evolution, as well as the process of species divergence, can be obtained in the absence of genomic sequence data, if the analysis is taken several steps beyond the standard phylogenetic tree construction approach. The main findings of the present study are these: The MHC class II B region of the passerine birds is as elaborate in its organization, divergence, and genetic diversity as the MHC of the eutherian mammals, specifically the primates. Hence, the reported simplicity of the fowl MHC is an oddity. With the help of appropriate markers, the divergence of the MHC genes can be traced deep in the phylogeny of the bird taxa. Transspecies polymorphism is rampant at many of the bird MHC loci. In this respect, the DFs behave as if they were a single, genetically undifferentiated population. There is thus far no indication of alleles that could be considered species, genus, or even DF group specific. The implication of these findings is that DFs are in the midst of adaptive radiations, in which morphological differentiation into species is running ahead of genetic differentiation in genetic systems such as the MHC or the mitochondrial DNA. The radiations are so young that there has not been enough time to sort out polymorphisms at most of the loci among the morphologically differentiating species. These findings parallel those on Lake Victoria haplochromine fishes. Several of the DF MHC allelic lineages can be traced back to the MHC genes of the species Tiaris obscura, which we identified previously as the closest extant relative of DFs in continental America.
Full-text · Article · May 2011 · Molecular Biology and Evolution
[Show abstract][Hide abstract] ABSTRACT: 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 Darwin's 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.
Full-text · Article · Feb 2011 · Proceedings of the National Academy of Sciences
[Show abstract][Hide abstract] ABSTRACT: The genetic basis of variation in fitness of many organisms has been studied in the laboratory, but relatively little is known of fitness variation in natural environments or its causes. Lifetime fitness (recruitment) may be determined solely by producing many offspring, modified by stochastic effects on their subsequent survival up to the point of breeding, or by an additional contribution made by the high quality of the offspring owing to nonrandom mate choice. To investigate the determinants of lifetime fitness, we measured offspring production, longevity, and lifetime number of mates in four cohorts of two long-lived species of socially monogamous Darwin's finch species, Geospiza fortis and G. scandens, on the equatorial Galápagos Island of Daphne Major. Regression analysis showed that the lifetime production of fledglings was predicted by lifetime number of clutches and that recruitment was predicted by lifetime number of fledglings and longevity. There was little support for a hypothesis of selective mating by females. The offspring sired by extrapair mates were no more fit in terms of recruitment than were half-sibs sired by social mates. These findings provide insight into the evolution of life history strategies of tropical birds. Darwin's finches deviate from the standard tropical pattern of a slow pace of life by combining tropical (long lifespan) and temperate (large clutch size) characteristics. Our study of fitness shows why this is so in terms of selective pressures (fledgling production and adult longevity) and ecological opportunities (pulsed food supply and relatively low predation).
Preview · Article · Jan 2011 · Proceedings of the National Academy of Sciences
[Show abstract][Hide abstract] ABSTRACT: Bird species sing different songs and as a result rarely breed with each other. Species are not static but can shift in acoustic and morphological space, yet maintain their distinctiveness. Investigating such a situation in a community of Darwin's finches sheds light on the origin and maintenance of premating barriers between species. Explanations for songs divergence generally invoke morphological changes to the sound-producing apparatus, environmental changes influencing transmitting properties of song, avoidance of acoustical interference with other species, and random processes including copying errors. We investigated changes in songs of Geospiza fortis (medium ground finch) and Geospiza scandens (cactus ground finch) from 1978 to 2010 on Daphne Major Island, Galápagos. The habitat did not change significantly; however, the finch community changed. The socially aggressive congener Geospiza magnirostris (large ground finch), singing in the same frequency band (2-4 kHz), colonized Daphne in 1983 and increased in numbers. Temporal features of the songs of G. fortis and G. scandens, especially trill rate and song duration, diverged from G. magnirostris songs as it became increasingly common. Changes in song were not a passive consequence of a change in beak morphology. Instead they arose as a bias during song imprinting and production. Sons of both G. fortis and G. scandens sang faster songs than their respective fathers and thereby differed more from G. magnirostris in their songs than did their fathers. Divergence from an aversive or confusing stimulus during learning illustrates a "peak shift" that may be a common feature of song evolution and speciation.
Preview · Article · Nov 2010 · Proceedings of the National Academy of Sciences
[Show abstract][Hide abstract] ABSTRACT: Genetic analysis of museum specimens offers a direct window into a past that can predate the loss of extinct forms. We genotyped 18 Galápagos finches collected by Charles Darwin and companions during the voyage of the Beagle in 1835, and 22 specimens collected in 1901. Our goals were to determine if significant genetic diversity has been lost since the Beagle voyage and to determine the genetic source of specimens for which the collection locale was not recorded. Using 'ancient' DNA techniques, we quantified variation at 14 autosomal microsatellite loci. Assignment tests showed several museum specimens genetically matched recently field-sampled birds from their island of origin. Some were misclassified or were difficult to classify. Darwin's exceptionally large ground finches (Geospiza magnirostris) from Floreana and San Cristóbal were genetically distinct from several other currently existing populations. Sharp-beaked ground finches (Geospiza difficilis) from Floreana and Isabela were also genetically distinct. These four populations are currently extinct, yet they were more genetically distinct from congeners than many other species of Darwin's finches are from each other. We conclude that a significant amount of the finch biodiversity observed and collected by Darwin has been lost since the voyage of the Beagle.
Preview · Article · Apr 2010 · Philosophical Transactions of The Royal Society B Biological Sciences
[Show abstract][Hide abstract] ABSTRACT: This study addresses the extent and consequences of gene exchange between populations of Darwin's finches. Four species of ground finches (Geospiza) inhabit the small island of Daphne Major in the centre of the Galápagos archipelago. We undertook a study of microsatellite DNA variation at 16 loci in order to quantify gene flow within species owing to immigration and between species owing to hybridization. A combination of pedigrees of observed breeders and assignments of individuals to populations by the program Structure enabled us to determine the frequency of gene exchange and the island of origin of immigrants in some cases. The relatively large populations of Geospiza fortis and G. scandens receive conspecific immigrants at a rate of less than one per generation. They exchange genes more frequently by rare but repeated hybridization. Effects of heterospecific gene flow from hybridization are not counteracted by lower fitness of the offspring. As a result, the standing genetic variation of the two main resident populations on Daphne Major is enhanced to a greater extent by introgressive hybridization than through breeding with conspecific immigrants. Immigrant G. fuliginosa also breeds with G. fortis. Conspecific immigration was highest in the fourth species, G. magnirostris. This species is much larger than the other three and perhaps for this reason it has not bred with any of them. The source island of most immigrants is probably the neighbouring island of Santa Cruz. Evolutionary change may be inhibited in G. magnirostris by continuing gene flow, but enhanced in G. fortis and G. scandens by introgressive hybridization.
Preview · Article · Apr 2010 · Philosophical Transactions of The Royal Society B Biological Sciences
[Show abstract][Hide abstract] ABSTRACT: Invasive parasites are a major threat to island populations of animals. Darwin's finches of the Galápagos Islands are under attack by introduced pox virus (Poxvirus avium) and nest flies (Philornis downsi). We developed assays for parasite-specific antibody responses in Darwin's finches (Geospiza fortis), to test for relationships between adaptive immune responses to novel parasites and spatial-temporal variation in the occurrence of parasite pressure among G. fortis populations.
We developed enzyme-linked immunosorbent assays (ELISAs) for the presence of antibodies in the serum of Darwin's finches specific to pox virus or Philornis proteins. We compared antibody levels between bird populations with and without evidence of pox infection (visible lesions), and among birds sampled before nesting (prior to nest-fly exposure) versus during nesting (with fly exposure). Birds from the Pox-positive population had higher levels of pox-binding antibodies. Philornis-binding antibody levels were higher in birds sampled during nesting. Female birds, which occupy the nest, had higher Philornis-binding antibody levels than males. The study was limited by an inability to confirm pox exposure independent of obvious lesions. However, the lasting effects of pox infection (e.g., scarring and lost digits) were expected to be reliable indicators of prior pox infection.
This is the first demonstration, to our knowledge, of parasite-specific antibody responses to multiple classes of parasites in a wild population of birds. Darwin's finches initiated acquired immune responses to novel parasites. Our study has vital implications for invasion biology and ecological immunology. The adaptive immune response of Darwin's finches may help combat the negative effects of parasitism. Alternatively, the physiological cost of mounting such a response could outweigh any benefits, accelerating population decline. Tests of the fitness implications of parasite-specific immune responses in Darwin's finches are urgently needed.
[Show abstract][Hide abstract] ABSTRACT: The distribution of mockingbird species among the Gala´pagos Islands prompted Charles Darwin to question, for the first time in writing, the ‘stability of species’. Some 50 years after Darwin’s visit, however, the endemic Floreana mockingbird (Mimus trifasciatus) had become extinct on Floreana Island and, today, only two small populations survive on two satellite islets. As Darwin noted, rarity often precedes extinction. To avert extinction, plans are being developed to reintroduce M. trifasciatus to Floreana. Here, we integrate evolutionary thinking and conservation practice using coalescent
analyses and genetic data from contemporary and museum samples, including two collected by Darwin and Robert Fitzroy on Floreana in 1835. Our microsatellite results show substantial differentiation between the two extant populations, but our coalescence-based modelling does not indicate long, independent evolutionary histories. One of the populations is highly inbred, but both harbour unique alleles present on Floreana in 1835, suggesting that birds from both islets should be used to establish a single, mixed population on Floreana. Thus, Darwin’s mockingbird specimens not only revealed to him a level of variation that suggested speciation following geographical isolation but also, more than 170 years later, return important information to their place of origin for the conservation of their conspecifics.