Ecological and morphological determinants of evolutionary diversification in Darwin's finches and their relatives

Darwin''s finches are a classic example of adaptive radiation, a process by which multiple ecologically distinct species rapidly evolve from a single ancestor. Such evolutionary diversification is typically explained by adaptation to new ecological opportunities. However, the ecological diversification of Darwin''s finches following their dispersal to Galápagos was not matched on the same archipelago by other lineages of colonizing land birds, which diversified very little in terms of both species number and morphology. To better understand the causes underlying the extraordinary variation in Darwin''s finches, we analyze the evolutionary dynamics of speciation and trait diversification in Thraupidae, including Coerebinae (Darwin''s finches and relatives) and, their closely related clade, Sporophilinae. For all traits, we observe an early pulse of speciation and morphological diversification followed by prolonged periods of slower steady‐state rates of change. The primary exception is the apparent recent increase in diversification rate in Darwin''s finches coupled with highly variable beak morphology, a potential key factor explaining this adaptive radiation. Our observations illustrate how the exploitation of ecological opportunity by contrasting means can produce clades with similarly high diversification rate yet strikingly different degrees of ecological and morphological differentiation.     

A phylogeny of Darwin's finches based on microsatellite DNA length variation

Allele length variation at 16 microsatellite loci was used to estimate the phylogeny of 13 out of the 14 species of Darwin''s finches. The resulting topology was similar to previous phylogenies based on morphological and allozyme variation. An unexpected result was that genetic divergence among Galápagos Island populations of the warbler finch (Certhidea olivacea) predates the radiation of all other Darwin''s finches. This deep split is surprising in view of the relatively weak morphological differentiation among Certhidea populations and supports the hypothesis that the ancestor of all Darwin''s finches was phenotypically similar to Certhidea. The results also resolve a biogeographical problem: the Cocos Island finch evolved after the Galápagos finch radiation was under way, supporting the hypothesis that this distant island was colonized from the Galápagos Islands. Monophyletic relationships are supported for both major groups, the ground finches (Geospiza) and the tree finches (Camarhynchus and Cactospiza), although the vegetarian finch (Platyspiza crassirostris) appears to have diverged prior to the separation of ground and tree finches. These results demonstrate the use of microsatellites for reconstructing phylogenies of closely related species and interpreting their evolutionary and biogeographic histories.     

Feeding innovations in a nested phylogeny of Neotropical passerines

Several studies on cognition, molecular phylogenetics and taxonomic diversity independently suggest that Darwin''s finches are part of a larger clade of speciose, flexible birds, the family Thraupidae, a member of the New World nine-primaried oscine superfamily Emberizoidea. Here, we first present a new, previously unpublished, dataset of feeding innovations covering the Neotropical region and compare the stem clades of Darwin''s finches to other neotropical clades at the levels of the subfamily, family and superfamily/order. Both in terms of raw frequency as well as rates corrected for research effort and phylogeny, the family Thraupidae and superfamily Emberizoidea show high levels of innovation, supporting the idea that adaptive radiations are favoured when the ancestral stem species were flexible. Second, we discuss examples of innovation and problem-solving in two opportunistic and tame Emberizoid species, the Barbados bullfinch Loxigilla barbadensis and the Carib grackle Quiscalus lugubris fortirostris in Barbados. We review studies on these two species and argue that a comparison of L. barbadensis with its closest, but very shy and conservative local relative, the black-faced grassquit Tiaris bicolor, might provide key insights into the evolutionary divergence of cognition.     

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.     

Darwin's Galápagos finches in modern biology

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.     

Human activity can influence the gut microbiota of Darwin's finches in the Galapagos Islands

The gut microbiota of animal hosts can be influenced by environmental factors, such as unnatural food items that are introduced by humans. Over the past 30 years, human presence has grown exponentially in the Galapagos Islands, which are home to endemic Darwin's finches. Consequently, humans have changed the environment and diet of Darwin's finches, which in turn, could affect their gut microbiota. In this study, we compared the gut microbiota of two species of Darwin's finches, small ground finches (Geospiza fuliginosa) and medium ground finches (Geospiza fortis), across sites with and without human presence, where finches prefer human‐processed and natural food, respectively. We predicted that: (a) finch microbiota would differ between sites with and without humans due to differences in diet, and (b) gut microbiota of each finch species would be most similar where finches have the highest niche overlap (areas with humans) compared to the lowest niche overlap (areas without humans). We found that gut bacterial community structure differed across sites and host species. Gut bacterial diversity was most distinct between the two species at the site with human presence compared to the site without human presence, which contradicted our predictions. Within host species, medium ground finches had lower bacterial diversity at the site with human presence compared to the site without human presence and bacterial diversity of small ground finches did not differ between sites. Our results show that the gut microbiota of Darwin's finches is affected differently across sites with varying human presence.     

THE MITOCHONDRIAL AND NUCLEAR GENETIC HOMOGENEITY OF THE PHENOTYPICALLY DIVERSE DARWIN'S GROUND FINCHES

The most extensively studied group of Darwin's finches is the genus Geospiza, the ground finches, and yet little is known about the evolutionary history and genetic relationships of these birds. Studies using either allozyme or morphological data have been unable to resolve relationships between the six species and numerous populations of ground finches. In this paper we report the results of a study using mitochondrial control region and nuclear internal transcribed spacer (ITS) 1 sequence data. The differentiation of the ground finch species based on morphological data is not reflected in either mitochondrial or nuclear DNA sequence phylogenies. Furthermore, there is little concordance between the mitochondrial haplotypes and ITS alleles found within individuals. We suggest that the absence of species-specific lineages can be attributed to ongoing hybridization involving all six species of Geospiza. There are no long term selective pressures against hybridization within this genus, and therefore a genetically homogenous genus may be maintained indefinitely. Hybridization has apparently played a role in the adaptive radiation of Darwin's finches.     

The adaptive genomic landscape of beak morphology in Darwin's finches

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.     

Multilocus genotypes from Charles Darwin's finches: biodiversity lost since the voyage of the Beagle

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.     

Evolutionary Dead End in the Galápagos: Divergence of Sexual Signals in the Rarest of Darwin's Finches

Understanding the mechanisms underlying speciation remains a challenge in evolutionary biology. The adaptive radiation of Darwin''s finches is a prime example of species formation, and their study has revealed many important insights into evolutionary processes. Here, we report striking differences in mating signals (songs), morphology and genetics between the two remnant populations of Darwin''s mangrove finch Camarhynchus heliobates, one of the rarest species in the world. We also show that territorial males exhibited strong discrimination of sexual signals by locality: in response to foreign songs, males responded weaker than to songs from their own population. Female responses were infrequent and weak but gave approximately similar results. Our findings not only suggest speciation in the mangrove finch, thereby providing strong support for the central role of sexual signals during speciation, but they have also implications for the conservation of this iconic bird. If speciation is complete, the eastern species will face imminent extinction, because it has a population size of only 5–10 individuals.     

Experimental demonstration of the fitness consequences of an introduced parasite of Darwin's finches

Background

Introduced parasites are a particular threat to small populations of hosts living on islands because extinction can occur before hosts have a chance to evolve effective defenses. An experimental approach in which parasite abundance is manipulated in the field can be the most informative means of assessing a parasite''s impact on the host. The parasitic fly Philornis downsi, recently introduced to the Galápagos Islands, feeds on nestling Darwin''s finches and other land birds. Several correlational studies, and one experimental study of mixed species over several years, reported that the flies reduce host fitness. Here we report the results of a larger scale experimental study of a single species at a single site over a single breeding season.

Methodology/Principal Findings

We manipulated the abundance of flies in the nests of medium ground finches (Geospiza fortis) and quantified the impact of the parasites on nestling growth and fledging success. We used nylon nest liners to reduce the number of parasites in 24 nests, leaving another 24 nests as controls. A significant reduction in mean parasite abundance led to a significant increase in the number of nests that successfully fledged young. Nestlings in parasite-reduced nests also tended to be larger prior to fledging.

Conclusions/Significance

Our results confirm that P. downsi has significant negative effects on the fitness of medium ground finches, and they may pose a serious threat to other species of Darwin''s finches. These data can help in the design of management plans for controlling P. downsi in Darwin''s finch breeding populations.     

Where did the finch go? Insights from radio telemetry of the medium ground finch (Geospiza fortis)

Movement patterns and habitat selection of animals have important implications for ecology and evolution. Darwin''s finches are a classic model system for ecological and evolutionary studies, yet their spatial ecology remains poorly studied. We tagged and radio‐tracked five (three females, two males) medium ground finches (Geospiza fortis) to examine the feasibility of telemetry for understanding their movement and habitat use. Based on 143 locations collected during a 3‐week period, we analyzed for the first time home‐range size and habitat selection patterns of finches at El Garrapatero, an arid coastal ecosystem on Santa Cruz Island (Galápagos). The average 95% home range and 50% core area for G. fortis in the breeding season was 20.54 ha ± 4.04 ha SE and 4.03 ha ± 1.11 ha SE, respectively. For most of the finches, their home range covered a diverse set of habitats. Three finches positively selected the dry‐forest habitat, while the other habitats seemed to be either negatively selected or simply neglected by the finches. In addition, we noted a communal roosting behavior in an area close to the ocean, where the vegetation is greener and denser than the more inland dry‐forest vegetation. We show that telemetry on Darwin''s finches provides valuable data to understand the movement ecology of the species. Based on our results, we propose a series of questions about the ecology and evolution of Darwin''s finches that can be addressed using telemetry.     

Ecoimmunity in Darwin's Finches: Invasive Parasites Trigger Acquired Immunity in the Medium Ground Finch (Geospiza fortis)

Background

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.

Methodology/Principal Findings

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.

Conclusions/Significance

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.     

Population genomics fits the bill: genetics of adaptive beak variation in Darwin's finches

Darwin's finches are an iconic case of adaptive radiation. The size and shape of their beaks are key adaptive traits related to trophic niche that vary among species and evolve rapidly when the food supply changes. Building on recent studies, a paper in this issue of Molecular Ecology (Chaves et al. 2016 ) investigates the genomic basis of beak size variation in sympatric populations of three species of ground finch (Geospiza) by performing a Genome‐wide association study using RAD‐seq data. The authors find that variation in a small number of markers can explain a substantial proportion of variation in beak size. Some of these markers are in genomic regions that have previously been implicated in beak size variation in Darwin's finches, whereas other markers have not, suggesting both conservation and divergence in the genetic basis of morphological evolution. Overall, the study confirms that loci of large effect are involved in beak size variation, which helps to explain the high heritability and rapid response to selection of this trait. The independent identification of regions containing HMGA2 and DLK1 loci in a GWAS makes them prime targets for functional studies. The study also shows that under the right conditions, RAD‐seq can be a viable alternative to genome sequencing for GWAS in wild vertebrate populations.     

Urbanization alters interactions between Darwin's finches and Tribulus cistoides on the Galápagos Islands

Emerging evidence suggests that humans shape the ecology and evolution of species interactions. Islands are particularly susceptible to anthropogenic disturbance due to the fragility of their ecosystems; however, we know little about the susceptibility of species interactions to urbanization on islands. To address this gap, we studied how the earliest stages of urban development affect interactions between Darwin''s finches and its key food resource, Tribulus cistoides, in three towns on the Galápagos Islands. We measured variation in mericarp predation rates, mericarp morphology, and finch community composition using population surveys, experimental manipulations, and finch observations conducted in habitats within and outside of each town. We found that both seed and mericarp removal rates were higher in towns than natural habitats. We also found that selection on mericarp size and defense differed between habitats in the survey and experimental populations and that towns supported smaller and less diverse finch communities than natural habitats. Together, our results suggest that even moderate levels of urbanization can alter ecological interactions between Darwin''s finches and T. cistoides, leading to modified natural selection on T. cistoides populations. Our study demonstrates that trophic interactions on islands may be susceptible to the anthropogenic disturbance associated with urbanization. Despite containing the highest diversity in the world, studies of urbanization are lacking from the tropics. Our study identified signatures of urbanization on species interactions in a tropical island ecosystem and suggests that changes to the ecology of species interactions has the potential to alter evolution in urban environments.     

Is Beak Morphology in Darwin’s Finches Tuned to Loading Demands?

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.     

Urban living influences the nesting success of Darwin’s finches in the Galápagos Islands

Urbanization is expanding worldwide with major consequences for organisms. Anthropogenic factors can reduce the fitness of animals but may have benefits, such as consistent human food availability. Understanding anthropogenic trade‐offs is critical in environments with variable levels of natural food availability, such as the Galápagos Islands, an area of rapid urbanization. For example, during dry years, the reproductive success of bird species, such as Darwin''s finches, is low because reduced precipitation impacts food availability. Urban areas provide supplemental human food to finches, which could improve their reproductive success during years with low natural food availability. However, urban finches might face trade‐offs, such as the incorporation of anthropogenic debris (e.g., string, plastic) into their nests, which may increase mortality. In our study, we determined the effect of urbanization on the nesting success of small ground finches (Geospiza fuliginosa; a species of Darwin''s finch) during a dry year on San Cristóbal Island. We quantified nest building, egg laying and hatching, and fledging in an urban and nonurban area and characterized the anthropogenic debris in nests. We also documented mortalities including nest trash‐related deaths and whether anthropogenic materials directly led to entanglement‐ or ingestion‐related nest mortalities. Overall, urban finches built more nests, laid more eggs, and produced more fledglings than nonurban finches. However, every nest in the urban area contained anthropogenic material, which resulted in 18% nestling mortality while nonurban nests had no anthropogenic debris. Our study showed that urban living has trade‐offs: urban birds have overall higher nesting success during a dry year than nonurban birds, but urban birds can suffer mortality from anthropogenic‐related nest‐materials. These results suggest that despite potential costs, finches benefit overall from urban living and urbanization may buffer the effects of limited resource availability in the Galápagos Islands.     

基于功能性状的外来植物入侵预测模型框架构建

预测外来植物的潜在入侵性已成为生物多样性保护研究的重要内容,外来植物与乡土物种间的亲缘关系是预测外来植物能否成功入侵的一个重要途径。然而,达尔文归化难题却预测了两种截然不同的结果(即达尔文归化假说和预适应假说)。该研究解析了达尔文归化难题的内涵,提出了基于功能性状的外来植物与乡土群落间的相似性关系应该是进行外来植物入侵预测的重要切入点,而功能性状的种间分化与种内变异可能是外来植物成功入侵的两种不同生态策略。在此基础上,该研究还通过物种功能性状的多维超体积构建了外来植物与乡土群落间的相似性,提出了基于这种相似性的外来植物入侵预测的研究框架和基本流程。该模型框架的建立有助于理解外来植物的入侵机制,对外来植物的潜在入侵性预测提供了理论依据。当然,要实现外来植物能否成功入侵的准确预测,不仅依赖于功能性状的选择,还要考虑入侵的生境依赖性、空间尺度的重要性以及乡土群落的可入侵性等,未来的研究重点是通过控制实验对该模型进行验证和进一步完善。     

THE EVOLUTIONARY HISTORY OF DARWIN'S FINCHES: SPECIATION,GENE FLOW,AND INTROGRESSION IN A FRAGMENTED LANDSCAPE

Many classic examples of adaptive radiations take place within fragmented systems such as islands or mountains, but the roles of mosaic landscapes and variable gene flow in facilitating species diversification is poorly understood. Here we combine phylogenetic and landscape genetic approaches to understand diversification in Darwin's finches, a model adaptive radiation. We combined sequence data from 14 nuclear introns, mitochondrial markers, and microsatellite variation from 51 populations of all 15 recognized species. Phylogenetic species‐trees recovered seven major finch clades: ground, tree, vegetarian, Cocos Island, grey and green warbler finches, and a distinct clade of sharp‐beaked ground finches (Geospiza cf. difficilis) basal to all ground and tree finches. The ground and tree finch clades lack species‐level phylogenetic structure. Interisland gene flow and interspecies introgression vary geographically in predictable ways. First, several species exhibit concordant patterns of population divergence across the channel separating the Galápagos platform islands from the separate volcanic province of northern islands. Second, peripheral islands have more admixed populations while central islands maintain more distinct species boundaries. This landscape perspective highlights a likely role for isolation of peripheral populations in initial divergence, and demonstrates that peripheral populations may maintain genetic diversity through outbreeding during the initial stages of speciation.     

Host‐specific associations affect the microbiome of Philornis downsi,an introduced parasite to the Galápagos Islands

The composition and diversity of bacteria forming the microbiome of parasitic organisms have implications for differential host pathogenicity and host–parasite co‐evolutionary interactions. The microbiome of pathogens can therefore have consequences that are relevant for managing disease prevalence and impact on affected hosts. Here, we investigate the microbiome of an invasive parasitic fly Philornis downsi, recently introduced to the Galápagos Islands, where it poses extinction threat to Darwin's finches and other land birds. Larvae infest nests of Darwin's finches and consume blood and tissue of developing nestlings, and have severe mortality impacts. Using 16s rRNA sequencing data, we characterize the bacterial microbiota associated with P. downsi adults and larvae sourced from four finch host species, inhabiting two islands and representing two ecologically distinct groups. We show that larval and adult microbiomes are dominated by the phyla Proteobacteria and Firmicutes, which significantly differ between life stages in their distributions. Additionally, bacterial community structure significantly differed between larvae retrieved from strictly insectivorous warbler finches (Certhidea olivacea) and those parasitizing hosts with broader dietary preferences (ground and tree finches, Geospiza and Camarhynchus spp., respectively). Finally, we found no spatial effects on the larval microbiome, as larvae feeding on the same host (ground finches) harboured similar microbiomes across islands. Our results suggest that the microbiome of P. downsi changes during its development, according to dietary composition or nutritional needs, and is significantly affected by host‐related factors during the larval stage. Unravelling the ecological significance of bacteria for this parasite will contribute to the development of novel, effective control strategies.