Naris and beak malformation caused by the parasitic fly, Philornis downsi (Diptera: Muscidae), in Darwin's small ground finch, Geospiza fuliginosa (Passeriformes: Emberizidae)

Parasites induce phenotypic modifications in their hosts, which can compromise host fitness. For example, the parasitic fly Philornis downsi , which was recently introduced to the Galápagos Islands, causes severe naris and beak malformation in Darwin's finches. The fly larvae feed on tissues from the nares of developing finch nestlings, thereby altering the size and shape of the nares and beak. Although the parasitism is age-specific (adult finches are not parasitized), naris and beak malformations persist into adulthood as parasite-induced malformations. We systematically examined adult populations of Darwin's small ground finch, Geospiza fuliginosa , on the islands of Santa Cruz for P. downsi -induced malformation. We found that malformed birds had significantly longer nares, and shorter, shallower beaks, than birds considered to be normal (i.e. with no nares or beak malformation). In addition, normal birds showed an isometry between naris length and beak dimensions (beak length feather and beak depth), which was not found in malformed birds. These differences suggest that beak morphology was influenced by P. downsi parasitism. Interestingly, we did not find any evidence of developmental impairment (smaller body size) or reduced foraging efficiency (lower body condition) between normal and malformed birds. Our findings of P. downsi -induced malformation raise new questions about the evolutionary trajectory and conservation status for this group of birds.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 577–585.     

Beak morphology and song features covary in a population of Darwin's finches (Geospiza fortis)

Animal mating signals evolve in part through indirect natural selection on anatomical traits that influence signal expression. In songbirds, for example, natural selection on beak form and function can influence the evolution of song features, because of the role of the beak in song production. In this study we characterize the relationship between beak morphology and song features within a bimodal population of Geospiza fortis on Santa Cruz Island, Galápagos. This is the only extant population of Darwin's finches that is known to possess a bimodal distribution in beak size. We test the hypothesis that birds with larger beaks are constrained to produce songs with lower frequencies and decreased vocal performance. We find that birds with longer, deeper, and wider beaks produce songs with significantly lower minimum frequencies, maximum frequencies and frequency bandwidths. Results from the analysis of the relationship between beak morphology and trill rate are mixed. Measures of beak morphology correlated positively with 'vocal deviation', a composite index of vocal performance. Overall these results support a resonance model of vocal tract function, and suggest that beak morphology, a primary target of ecological selection in Darwin's finches, affects the evolution of mating signals. We suggest that differences in song between the two modes of the distribution may influence mate recognition and perhaps facilitate assortative mating by beak size and population divergence.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 88 , 489–498.     

Evolution of bite force in Darwin's finches: a key role for head width

Studies of Darwin's finches of the Galapagos Islands have provided pivotal insights into the interplay of ecological variation, natural selection, and morphological evolution. Here we document, across nine Darwin's finch species, correlations between morphological variation and bite force capacity. We find that bite force correlates strongly with beak depth and width but only weakly or not at all with beak length, a result that is consistent with prior demonstrations of natural selection on finch beak morphology. We also find that bite force is predicted even more strongly by head width, which exceeds all beak dimensions in predictive strength. To explain this result we suggest that head width determines the maximum size, and thus maximum force generation capacity of finch jaw adductor muscles. We suggest that head width is functionally relevant and may be a previously unrecognized locus of natural selection in these birds, because of its close relationship to bite force capacity.     

A geometric morphometric appraisal of beak shape in Darwin's finches

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.     

Phylogenetic relationships and morphological diversity in Darwin's finches and their relatives

Despite the importance of Darwin's finches to the development of evolutionary theory, the origin of the group has only recently been examined using a rigorous, phylogenetic methodology that includes many potential outgroups. Knowing the evolutionary relationships of Darwin's finches to other birds is important for understanding the context from which this adaptive radiation arose. Here we show that analysis of mitochondrial DNA sequence data from the cytochrome b gene confirm that Darwin's finches are monophyletic. In addition, many taxa previously proposed as the sister taxon to Darwin's finches can be excluded as their closest living relative. Darwin's finches are part of a well-supported monophyletic group of species, all of which build a domed nest. All but two of the non-Darwin's finches included in this clade occur on Caribbean islands and most are Caribbean endemics. These close relatives of Darwin's finches show a diversity of bill types and feeding behaviors similar to that observed among Darwin's finches themselves. Recent studies have shown that adaptive evolution in Darwin's finches occurred relatively quickly. Our data show that among the relatives of Darwin's finches, the evolution of bill diversity was also rapid and extensive.     

On the origin of Darwin's finches

Darwin's finches comprise a group of 15 species endemic to the Galápagos (14 species) and Cocos (1 species) Islands in the Pacific Ocean. The group is monophyletic and originated from an ancestral species that reached the Galápagos Archipelago from Central or South America. Descendants of this ancestor on the Archipelago then colonized Cocos Island. In the present study, we used sequences of two mitochondrial (mt) DNA segments (922 bp of the cytochrome b gene and 1,082 bp of the control region), as well as two nuclear markers (830 bp of numt2, consisting of 140 bp of mtDNA control region and 690 bp of flanking nuclear DNA; and 740 bp of numt3, consisting of 420 bp of mt cytochrome b sequence flanked by 320 bp of nuclear DNA) to identify the species group most closely related to the Darwin's finches. To this end, we analyzed the sequences of 28 species representing the main groups (tribes) of the family Fringillidae, as well as 2 outgroup species and 13 species of Darwin's finches. In addition, we used mtDNA cytochrome b sequences of some 180 additional Fringillidae species from the database for phylogeny reconstruction by maximum-parsimony, maximum-likelihood, minimum-evolution, and neighbor-joining methods. The study identifies the grassquit genus Tiaris, and specifically the species Tiaris obscura, as the nearest living relative of Darwin's finches among the species surveyed. Darwin's finches diverged from the Tiaris group shortly after the various extant species of Tiaris diverged from one another. The initial adaptive radiation of the Tiaris group apparently occurred on the Caribbean islands and then spread to Central and South America, from where the ancestors of Darwin's finches departed for the Galápagos Islands approximately 2.3 MYA, at the time of the dramatic climatic changes associated with the closure of the Panamanian isthmus and the onset of Pleistocene glaciation.     

Recent research on the evolution of land birds on the Galápagos

A decade of research on the evolution of Galápagos land birds is reviewed, and outstanding questions to be answered are highlighted. Evolutionary studies have been restric 1 almost entirely to the four species of mockingbirds and the 13 species of Darwin's finches. Long-term field studies have been initiated on representatives of both groups. Co-operative breeding has been discovered in the mockingbirds (and hawks).
Lack's (1945, 1947) monographic treatment of Darwin's finches has been largely upheld and extended by morphological, ecological, behavioural and biochemical studies. While the phylogenetic origins of Darwin's finches still remain uncertain, the major groupings of the finches have been confirmed by the results of protein polymorphism analysis. Fossils of Darwin's finches have been discovered recently: their potential for illuminating evolutionary change has not yet been realized. Three other major developments are (1) quantitative confirmation of the role of interspecific competition in the adaptive radiation, (2) experimental confirmation of the role of morphological and song cues in species recognition, and experimental evidence of their evolution in the speciation process, and (3) direct study of natural selection on heritable quantitative traits in a population, and identification of its causes. Continuing studies of population variation are likely to reveal the contemporary importance of selection, migration and hybridization, and thereby help us to more fully understand the causes of the adaptive radiation of Darwin's finches.     

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 Darwin's finches. We compare the three most genetically divergent groups of Darwin's 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 Darwin's 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 Lack's two-stage model of speciation: relative ecological stasis in allopatry followed by secondary contact, ecological interactions and asymmetric phenotypic divergence.     

Reproductive isolation of sympatric morphs in a population of Darwin's finches

Recent research on speciation has identified a central role for ecological divergence, which can initiate speciation when (i) subsets of a species or population evolve to specialize on different ecological resources and (ii) the resulting phenotypic modes become reproductively isolated. Empirical evidence for these two processes working in conjunction, particularly during the early stages of divergence, has been limited. We recently described a population of the medium ground finch, Geospiza fortis, that features large and small beak morphs with relatively few intermediates. As in other Darwin's finches of the Galápagos Islands, these morphs presumably diverged in response to variation in local food availability and inter- or intraspecific competition. We here demonstrate that the two morphs show strong positive assortative pairing, a pattern that holds over three breeding seasons and during both dry and wet conditions. We also document restrictions on gene flow between the morphs, as revealed by genetic variation at 10 microsatellite loci. Our results provide strong support for the central role of ecology during the early stages of adaptive radiation.     

Adaptive significance of avian beak morphology for ectoparasite control

The beaks of Darwin's finches and other birds are among the best known examples of adaptive evolution. Beak morphology is usually interpreted in relation to its critical role in feeding. However, the beak also plays an important role in preening, which is the first line of defence against harmful ectoparasites such as feather lice, fleas, bugs, flies, ticks and feather mites. Here, we show a feature of the beak specifically adapted for ectoparasite control. Experimental trimming of the tiny (1-2 mm) maxillary overhang of rock pigeons (Columba livia) had no effect on feeding efficiency, yet triggered a dramatic increase in feather lice and the feather damage they cause. The overhang functions by generating a shearing force against the tip of the lower mandible, which moves forward remarkably quickly during preening, at up to 31 timesper second. This force damages parasite exoskeletons, significantly enhancing the efficiency of preening for parasite control. Overhangs longer than the natural mean of 1.6mm break significantly more often than short overhangs. Hence, stabilizing selection will favour overhangs of intermediate length. The adaptive radiation of beak morphology should be re-assessed with both feeding and preening in mind.     

Population variation and hybridization: Comparison of finches from two archipelagos

Summary Some populations of Darwin's Finches (Emberizinae) are exceptionally variable in body size and beak traits as a result of introgressive hybridization. A study of museum specimens of honeycreeper-finches (Carduelinae) from the Hawaiian islands was undertaken to see if the same phenomenon was manifested by a different phyletic group of finches in a different archipelago. Five hundred and twenty-four specimens of the seven species with finch-like bills were measured and their coefficients of variation were compared with those of the ground finch group (six species) of Darwin's Finches. Coefficients were smaller in the Hawaiian finches. Sympatric and, hence, potentially hybridizing species on the island of Hawaii were not consistently more variable than the allopatric species on other islands in the archipelago. The one species with both sympatric and allopatric populations did not show greater variation in the sympatric population. There is little evidence from these comparisons of hybridization occurring in the last 100 years. The difference between the two finch faunas can be explained in terms of two factors. Finches have been present for a longer time in the Hawaiian archipelago than in the Galápagos archipelago and have had more time to not only diversify but to evolve pre- and post-zygotic isolating mechanisms. In the generally less seasonal and floristically richer Hawaiian islands they have evolved greater dietary specializations. Beak traits adapted to specialist feeding may have been under stronger stabilizing selection and hybrids (if formed) may have been at a strong disadvantage in the absence of an ecological niche intermediate between the niches of the two parental species. Results of published electrophoretic studies of genetic variation suggest that the early phase of differentiation, involving occasional introgressive hybridization, may last for up to 5 million years.     

Fission and fusion of Darwin's finches populations

This study addresses the causes and evolutionary consequences of introgressive hybridization in the sympatric species of Darwin's ground finches (Geospiza) on the small island of Daphne Major in the Galápagos archipelago. Hybridization occurs rarely (less than 2% of breeding pairs) but persistently across years, usually as a result of imprinting on the song of another species. Hybrids survive well under some ecological conditions, but not others. Hybrids mate according to song type. The resulting introgression increases phenotypic and genetic variation in the backcrossed populations. Effects of introgression on beak shape are determined by the underlying developmental genetic pathways. Introgressive hybridization has been widespread throughout the archipelago in the recent past, and may have been a persistent feature throughout the early history of the radiation, episodically affecting both the speed and direction of evolution. We discuss how fission through selection and fusion through introgression in contemporary Darwin's finch populations may be a reflection of processes occurring in other young radiations. We propose that introgression has the largest effect on the evolution of interbreeding species after they have diverged in morphology, but before the point is reached when genetic incompatibilities incur a severe fitness cost.     

Mechanical stress,fracture risk and beak evolution in Darwin's ground finches (Geospiza)

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.     

Beak of the pinch: anti-parasite traits are similar among Darwin’s finch species

Darwin’s finches are an iconic example of adaptive radiation. The size and shape of the beaks of different finch species are diversified for feeding on different size seeds and other food resources. However, beaks also serve other functions, such as preening for the control of ectoparasites. In diverse groups of birds, the effectiveness of preening is governed by the length of the overhanging tip of the upper mandible of the beak. This overhang functions as a template against which the tip of the lower mandible generates a pinching force sufficient to damage or kill ectoparasites. Here we compare feeding versus preening components of the beak morphology of small, medium, and large ground finches that share a single parasite community. Despite adaptive divergence in beak morphology related to feeding, the three species have nearly identical relative mandibular overhang lengths. Moreover, birds with intermediate length overhangs have the lowest feather mite loads. These results suggest that Darwin’s finches maintain an optimal beak morphology to effectively control their ectoparasites.     

The effect of capture-and-handling stress on carotenoid-based beak coloration in zebra finches

Stress can have widespread effects on animal behaviors and phenotypes, including sexually selected traits. Ornamental colors have long been studied as honest signals of condition, but few studies have been conducted on how the physiological stress response (i.e., corticosterone (CORT) elevation) impacts color expression. We used a traditional capture-and-restraint technique to examine the effect of repeated handling stress on carotenoid-dependent beak coloration in male and female zebra finches (Taeniopygia guttata). Birds subjected to daily, 10-min handling treatments, which elevated circulating CORT levels, for a four-week period displayed deeper orange/red beak coloration than did control animals. Stressed males lost body mass during the experiment and marginally decreased in circulating carotenoid concentrations. Hence, handling stress may have reduced food intake or induced mobilization of body stores (i.e., fat) of carotenoids. In contrast to males, stressed females maintained orange beak color, while control females faded in color. This study highlights sex- and pigment-specific mechanisms by which stress may temporarily enhance the expression of sexual traits, but at the expense of other key fitness traits (e.g., body mass maintenance, reproduction).     

Carotenoids, immunocompetence, and the information content of sexual colors: an experimental test

Many male birds use carotenoid pigments to acquire brilliant colors that advertise their health and condition to prospective mates. The direct means by which the most colorful males achieve superior health has been debated, however. One hypothesis, based on studies of carotenoids as antioxidants in humans and other animals, is that carotenoids directly boost the immune system of colorful birds. We studied the relationship between carotenoid pigments, immune function, and sexual coloration in zebra finches (Taeniopygia guttata), a species in which males incorporate carotenoid pigments into their beak to attract mates. We tested the hypotheses that increased dietary carotenoid intake enhances immunocompetence in male zebra finches and that levels of carotenoids circulating in blood, which also determine beak coloration, directly predict the immune response of individuals. We experimentally supplemented captive finches with two common dietary carotenoid pigments (lutein and zeaxanthin) and measured cell-mediated and humoral immunity a month later. Supplemented males showed elevated blood-carotenoid levels, brighter beak coloration, and increased cell-mediated and humoral immune responses than did controls. Cell-mediated responses were predicted directly by changes in beak color and plasma carotenoid concentration of individual birds. These experimental findings suggest that carotenoid-based color signals in birds may directly signal male health via the immunostimulatory action of ingested and circulated carotenoid pigments.     

Divergence with gene flow as facilitated by ecological differences: within-island variation in Darwin's finches

Divergence and speciation can sometimes proceed in the face of, and even be enhanced by, ongoing gene flow. We here study divergence with gene flow in Darwin''s finches, focusing on the role of ecological/adaptive differences in maintaining/promoting divergence and reproductive isolation. To this end, we survey allelic variation at 10 microsatellite loci for 989 medium ground finches (Geospiza fortis) on Santa Cruz Island, Galápagos. We find only small genetic differences among G. fortis from different sites. We instead find noteworthy genetic differences associated with beak. Moreover, G. fortis at the site with the greatest divergence in beak size also showed the greatest divergence at neutral markers; i.e. the lowest gene flow. Finally, morphological and genetic differentiation between the G. fortis beak-size morphs was intermediate to that between G. fortis and its smaller (Geospiza fuliginosa) and larger (Geospiza magnirostris) congeners. We conclude that ecological differences associated with beak size (i.e. foraging) influence patterns of gene flow within G. fortis on a single island, providing additional support for ecological speciation in the face of gene flow. Patterns of genetic similarity within and between species also suggest that interspecific hybridization might contribute to the formation of beak-size morphs within G. fortis.     

Increasing prevalence of avian poxvirus in Darwin's finches and its effect on male pairing success

Island populations harbour a comparatively species-poor pathogen community, often resulting in naïve host species that experience compromised immunity when faced with novel diseases. Over 95% of the Galápagos avifauna have survived 400 years of human settlement, yet currently face threats due to introduced diseases such as avian poxvirus. On Hawaii, declining populations of birds and even some extinctions have been attributed to avian poxvirus, and hence, identifying the prevalence and fitness costs of avian poxvirus on the Galápagos is a conservation priority. Surveys of avian poxvirus in Darwin's finches on Santa Cruz Island between 2000 and 2004 found a 33% annual increase in the prevalence of pox lesions in ground finches. Comparisons of pox prevalence on three islands (Santa Cruz, Floreana, and Isabela) were made in 2004, which indicated significant variation in pox prevalence across islands (Isabela>Santa Cruz>Floreana). Darwin's finch species were found to be differentially affected by poxvirus, with a higher prevalence in ground finches than in tree finches. There was a significant effect of habitat, even within species, with higher prevalence in the lowlands than highlands. Pox prevalence was not correlated with sex or body condition. However, male small ground finches Geospiza fuliginosa with evidence of pox were less likely to have a mate (16.6% paired) compared with males without pox (77% paired), indicating fitness costs associated with poxvirus infection.     

Lack of premating isolation at the base of a phylogenetic tree

Darwin's finches in the Galápagos archipelago are an unusual example of adaptive radiation in that the basal split separates two lineages of warbler finches (Certhidea olivacea and Certhidea fusca) believed until recently to be only one species. The large genetic difference between them contrasts with their similarity in plumage, size, shape, and courtship behavior. They differ in song, which is a key factor in premating isolation of other sympatric Darwin's finches. We conducted playback experiments to see whether members of the population of C. olivacea on Santa Cruz Island would respond to songs of C. fusca from two islands, Genovesa and Pinta, and songs of C. olivacea from another island (Isabela). Another set of experiments was performed, using the same playback tapes, with C. fusca on Genovesa. Some members of both populations responded to all playbacks; therefore, the hypothesis of complete premating isolation on the basis of song is rejected. Discrimination between songs of the two lineages was inconsistent. We conclude that premating barriers to interbreeding among the tested populations have not arisen in the 1.5-2.0 m.yr. of their geographical isolation on different islands. This contrasts with strong premating barriers between more recently derived sympatric species. Early learning of song associated with morphology is later used in mate recognition. This explains why sympatric species that are vocally and morphologically distinct yet genetically less differentiated than Certhidea do not interbreed, whereas the Certhidea lineages that are genetically well differentiated but vocally and morphologically similar have no apparent premating barrier. We discuss this unusual situation in terms of the forces that have produced similarities and differences in song, morphology, and ecology and their relevance to phylogenetic and biological species concepts. Neither principles nor details are unique to Darwin's finches, and we conclude by pointing out strong parallels with some continental birds.