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The theory of ecological speciation posits that adaptive divergence among incipient species raises incidental barriers to reproduction, thus catalyzing the emergence of new species. In this study, we conducted an experimental test of this theory in Galápagos finches, a clade in which beaks and mating songs are mechanistically linked. We forecasted the acoustic structure of songs for a set of possible evolutionary futures (successive droughts spurring increasingly large beaks) and, in a field assay, presented resulting song simulations to territorial males. We found that responses to songs dropped off after six simulated drought events, to degrees roughly comparable to drops in response to songs that diverged through cultural drift and acoustic adaptation. Our results support, in Darwin's finches, the feasibility and mechanistic bases of an ecological speciation hypothesis.

A fundamental goal in evolutionary biology is to understand the genetic architecture of adaptive traits. Using whole-genome data of 3955 of Darwin's finches on the Galápagos Island of Daphne Major, we identified six loci of large effect that explain 45% of the variation in the highly heritable beak size of Geospiza fortis, a key ecological trait. The major locus is a supergene comprising four genes. Abrupt changes in allele frequencies at the loci accompanied a strong change in beak size caused by natural selection during a drought. A gradual change in Geospiza scandens occurred across 30 years as a result of introgressive hybridization with G. fortis . This study shows how a few loci with large effect on a fitness-related trait contribute to the genetic potential for rapid adaptive radiation.

Carotenoid-based polymorphisms are widespread in populations of birds, fish, and reptiles, 1 but generally little is known about the factors affecting their maintenance in populations. 2 We report a combined field and molecular-genetic investigation of a nestling beak color polymorphism in Darwin's finches. Beaks are pink or yellow, and yellow is recessive. 3 Here we show that the polymorphism arose in the Galápagos half a million years ago through a mutation associated with regulatory change in the BCO2 gene and is shared by 14 descendant species. The polymorphism is probably a balanced polymorphism, maintained by ecological selection associated with survival and diet. In cactus finches, the frequency of the yellow genotype is correlated with cactus fruit abundance and greater hatching success and may be altered by introgressive hybridization. Polymorphisms that are hidden as adults, as here, may be far more common than is currently recognized, and contribute to diversification in ways that are yet to be discovered., Competing Interests: Declaration of interests Authors declare no competing interests., (Copyright © 2021 The Authors. Published by Elsevier Inc. All rights reserved.)

Adaptive radiations are prominent components of the world's biodiversity. They comprise many species derived from one or a small number of ancestral species in a geologically short time that have diversified into a variety of ecological niches. Several authors have proposed that introgressive hybridization has been important in the generation of new morphologies and even new species, but how that happens throughout evolutionary history is not known. Interspecific gene exchange is expected to have greatest impact on variation if it occurs after species have diverged genetically and phenotypically but before genetic incompatibilities arise. We use a dated phylogeny to infer that populations of Darwin's finches in the Galápagos became more variable in morphological traits through time, consistent with the hybridization hypothesis, and then declined in variation after reaching a peak. Some species vary substantially more than others. Phylogenetic inferences of hybridization are supported by field observations of contemporary hybridization. Morphological effects of hybridization have been investigated on the small island of Daphne Major by documenting changes in hybridizing populations of Geospiza fortis and Geospiza scandens over a 30-y period. G. scandens showed more evidence of admixture than G. fortis Beaks of G. scandens became progressively blunter, and while variation in length increased, variation in depth decreased. These changes imply independent effects of introgression on 2, genetically correlated, beak dimensions. Our study shows how introgressive hybridization can alter ecologically important traits, increase morphological variation as a radiation proceeds, and enhance the potential for future evolution in changing environments., Competing Interests: The authors declare no competing interest.

Pyrenestes finches are unique among birds in showing a non-sex-determined polymorphism in bill size and are considered a textbook example of disruptive selection. Morphs breed randomly with respect to bill size, and differ in diet and feeding performance relative to seed hardness. Previous breeding experiments are consistent with the polymorphism being controlled by a single genetic factor. Here, we use genome-wide pooled sequencing to explore the underlying genetic basis of bill morphology and identify a single candidate region. Targeted resequencing reveals extensive linkage disequilibrium across a 300 Kb region containing the insulin-like growth factor 1 (IGF1) gene, with a single 5-million-year-old haplotype associating with phenotypic dominance of the large-billed morph. We find no genetic similarities controlling bill size in the well-studied Darwin's finches (Geospiza). Our results show how a single genetic factor may control bill size and provide a foundation for future studies to examine this phenomenon within and among avian species.

Beak shape in Darwin's ground finches (Geospiza) is emblematic of natural selection and adaptive radiation, yet our understanding of the genetic basis of beak shape variation, and thus the genetic target of natural selection, is still evolving. Here we reveal the genomic architecture of beak shape variation using genomewide comparisons of four closely related and hybridizing species across 13 islands subject to parallel natural selection. Pairwise contrasts among species were used to identify a large number of genomic loci that are consistently related to species differences across a complex landscape. These loci are associated with hundreds of genes that have enriched GO categories significantly associated with development. One genomic region of particular interest is a section of Chromosome 1A with many candidate genes and increased linkage. The distinct, pointed beak shape of the cactus finch is linked to an excess of intermediate frequency alleles and increased heterozygosity in significant SNPs, but not across the rest of the genome. Alleles associated with pointier beaks among species were associated with pointier-beaked populations within each species, thus establishing a common basis for natural selection, species divergence and adaptive radiation. The adaptive genomic landscape for Darwin's finches mirrors theoretical expectations based on morphological variation. The implication that a large number of genes are actively maintained to facilitate beak variation across parallel populations with documented interspecies admixture challenges our understanding of evolutionary processes in the wild., (© 2017 John Wiley & Sons Ltd.)

Ecological character displacement is a process of morphological divergence that reduces competition for limited resources. We used genomic analysis to investigate the genetic basis of a documented character displacement event in Darwin's finches on Daphne Major in the Galápagos Islands: The medium ground finch diverged from its competitor, the large ground finch, during a severe drought. We discovered a genomic region containing the HMGA2 gene that varies systematically among Darwin's finch species with different beak sizes. Two haplotypes that diverged early in the radiation were involved in the character displacement event: Genotypes associated with large beak size were at a strong selective disadvantage in medium ground finches (selection coefficient s = 0.59). Thus, a major locus has apparently facilitated a rapid ecological diversification in the adaptive radiation of Darwin's finches., (Copyright © 2016, American Association for the Advancement of Science.)

One of nature's premier illustrations of adaptive evolution concerns the tight correspondence in birds between beak morphology and feeding behavior. In seed-crushing birds, beaks have been suggested to evolve at least in part to avoid fracture. Yet, we know little about mechanical relationships between beak shape, stress dissipation, and fracture avoidance. This study tests these relationships for Darwin's finches, a clade of birds renowned for their diversity in beak form and function. We obtained anatomical data from micro-CT scans and dissections, which in turn informed the construction of finite element models of the bony beak and rhamphotheca. Our models offer two new insights. First, engineering safety factors are found to range between 1 and 2.5 under natural loading conditions, with the lowest safety factors being observed in species with the highest bite forces. Second, size-scaled finite element (FE) models reveal a correspondence between inferred beak loading profiles and observed feeding strategies (e.g. edge-crushing versus tip-biting), with safety factors decreasing for base-crushers biting at the beak tip. Additionally, we identify significant correlations between safety factors, keratin thickness at bite locations, and beak aspect ratio (depth versus length). These lines of evidence together suggest that beak shape indeed evolves to resist feeding forces.

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.

Quantitative trait locus (QTL) mapping is frequently used in evolutionary studies to understand the genetic architecture of continuously varying traits. The majority of studies have been conducted in specially created crosses, in which genetic differences between parental lines are identified by linkage analysis. Detecting QTL segregating within populations is more problematic, especially in wild populations, because these populations typically have complicated and unbalanced multigenerational pedigrees. However, QTL mapping can still be conducted in such populations using a variance components mixed model approach, and the advent of appropriate statistical frameworks and better genotyping methods mean that the approach is gaining popularity. In this study it is shown that all studies described to date report evidence of QTL of major effect on trait variation, but that these findings are probably caused by inflated estimates of QTL effect sizes due to the Beavis effect. Using simulations I show that even the most powerful studies conducted to date are likely to give misleading descriptions of the genetic architecture of a trait. I show that an interpretation of a mapping study of beak color in the zebra finch (Taeniopygia guttata), that suggested genetic variation was determined by a small number of loci of large effect, which are possibly maintained by antagonistic pleiotropy, is likely to be incorrect. More generally, recommendations are made to how QTL mapping can be combined with other approaches to provide more accurate descriptions of a trait's genetic architecture., (© 2013 The Author(s). Evolution © 2013 The Society for the Study of Evolution.)

The astonishing variation in the shape and size of bird beaks reflects a wide range of dietary specializations that played an important role in avian diversification. Among Darwin's finches, ground finches (Geospiza spp.) have beaks that represent scaling variations of the same shape, which are generated by alterations in the signaling pathways that regulate growth of the two skeletal components of the beak: the prenasal cartilage (pnc) and the premaxillary bone (pmx). Whether this developmental mechanism is responsible for variation within groups of other closely related bird species, however, has remained unknown. Here, we report that the Caribbean bullfinches (Loxigilla spp.), which are closely related to Darwin's finches, have independently evolved beaks of a novel shape, different from Geospiza, but also varying from each other only in scaling. However, despite sharing the same beak shape, the signaling pathways and tissues patterning Loxigilla beaks differ among the three species. In Loxigilla noctis, as in Geospiza, the pnc develops first, shaped by Bmp4 and CaM signaling, followed by the development of the pmx, regulated by TGFβIIr, β-catenin, and Dkk3 signaling. In contrast, beak morphogenesis in Loxigilla violacea and Loxigilla portoricensis is generated almost exclusively by the pmx through a mechanism in which Ihh and Bmp4 synergize to promote expansion of bone tissue. Together, our results demonstrate high flexibility in the relationship between morphology and underlying developmental causes, where different developmental programs can generate identical shapes, and similar developmental programs can pattern different shapes.

The intra- and interspecific diversity of avian beak morphologies is one of the most compelling examples for the power of natural selection acting on a morphological trait. The development and diversification of the beak have also become a textbook example for evolutionary developmental biology, and variation in expression levels of several genes is known to causally affect beak shape. However, until now, no genomic polymorphisms have been identified, which are related to beak morphology in birds. QTL mapping does reveal the location of causal polymorphisms, albeit with poor spatial resolution. Here, we estimate heritability and genetic correlations for beak length, depth and width and perform a QTL linkage analysis for these traits based on 1404 informative single-nucleotide polymorphisms genotyped in a four-generation pedigree of 992 captive zebra finches (Taeniopygia guttata). Beak size, relative to body size, was sexually dimorphic (larger in males). Heritability estimates ranged from 0.47 for beak length to 0.74 for beak width. QTL mapping revealed four to five regions of significant or suggestive genome-wide linkage for each of the three beak dimensions (nine different regions in total). Eight out of 11 genes known to influence beak morphology are located in these nine peak regions. Five QTL do not cover known candidates demonstrating that yet unknown genes or regulatory elements may influence beak morphology in the zebra finch., (© 2012 Blackwell Publishing Ltd.)

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.

One of the classic examples of adaptive radiation under natural selection is the evolution of 15 closely related species of Darwin's finches (Passeriformes), whose primary diversity lies in the size and shape of their beaks. Since Charles Darwin and other members of the Beagle expedition collected these birds on the Galápagos Islands in 1835 and introduced them to science, they have been the subjects of intense research. Many biology textbooks use Darwin's finches to illustrate a variety of topics of evolutionary theory, such as speciation, natural selection and niche partitioning. Today, as this Theme Issue illustrates, Darwin's finches continue to be a very valuable source of biological discovery. Certain advantages of studying this group allow further breakthroughs in our understanding of changes in recent island biodiversity, mechanisms of speciation and hybridization, evolution of cognitive behaviours, principles of beak/jaw biomechanics as well as the underlying developmental genetic mechanisms in generating morphological diversity. Our objective was to bring together some of the key workers in the field of ecology and evolutionary biology who study Darwin's finches or whose studies were inspired by research on Darwin's finches. Insights provided by papers collected in this Theme Issue will be of interest to a wide audience.

Darwin's finches have radiated from a common ancestor into 14 descendent species, each specializing on distinct food resources and evolving divergent beak forms. Beak morphology in the ground finches (Geospiza) has been shown to evolve via natural selection in response to variation in food type, food availability and interspecific competition for food. From a mechanical perspective, however, beak size and shape are only indirectly related to birds' abilities to crack seeds, and beak form is hypothesized to evolve mainly under selection for fracture avoidance. Here, we test the fracture-avoidance hypothesis using finite-element modelling. We find that across species, mechanical loading is similar and approaches reported values of bone strength, thus suggesting pervasive selection on fracture avoidance. Additionally, deep and wide beaks are better suited for dissipating stress than are more elongate beaks when scaled to common sizes and loadings. Our results illustrate that deep and wide beaks in ground finches enable reduction of areas with high stress and peak stress magnitudes, allowing birds to crack hard seeds while limiting the risk of beak failure. These results may explain strong selection on beak depth and width in natural populations of Darwin's finches.

The link between adaptation and evolutionary change remains the most central and least understood evolutionary problem. Rapid evolution and diversification of avian beaks is a textbook example of such a link, yet the mechanisms that enable beak's precise adaptation and extensive adaptability are poorly understood. Often observed rapid evolutionary change in beaks is particularly puzzling in light of the neo-Darwinian model that necessitates coordinated changes in developmentally distinct precursors and correspondence between functional and genetic modularity, which should preclude evolutionary diversification. I show that during first 19 generations after colonization of a novel environment, house finches (Carpodacus mexicanus) express an array of distinct, but adaptively equivalent beak morphologies-a result of compensatory developmental interactions between beak length and width in accommodating microevolutionary change in beak depth. Directional selection was largely confined to the elimination of extremes formed by these developmental interactions, while long-term stabilizing selection along a single axis-beak depth-was mirrored in the structure of beak's additive genetic covariance. These results emphasize three principal points. First, additive genetic covariance structure may represent a historical record of the most recurrent developmental and functional interactions. Second, adaptive equivalence of beak configurations shields genetic and developmental variation in individual components from depletion by natural selection. Third, compensatory developmental interactions among beak components can generate rapid reorganization of beak morphology under novel conditions and thus greatly facilitate both the evolution of precise adaptation and extensive diversification, thereby linking adaptation and adaptability in this classic example of Darwinian evolution.

Beak size and shape in Darwin's finches have traditionally been quantified using a few univariate measurements (length, depth, width). Here we show the improved inferential resolution of geometric morphometric methods, as applied to three hierarchical levels: (i) among seven species on Santa Cruz Island, (ii) among different sites on Santa Cruz for a single species (Geospiza fortis), and (iii) between large and small beak size morphs of G. fortis at one site (El Garrapatero). Our results support previous studies in finding an axis of shape variation (long/shallow/pointy vs. short/deep/blunt) that separates many of the species. We also detect additional differences among species in the relative sizes and positions of the upper and lower mandibles and in curvature of the mandibles. Small-scale, but potentially relevant, shape variation was also detected among G. fortis from different sites and between sympatric beak size morphs. These results suggest that adaptation to different resources might contribute to diversification on a single island.

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.