The genome sequence of the avian vampire fly (Philornis downsi), an invasive nest parasite of Darwin’s finches in Galápagos

The invasive avian vampire fly (Philornis downsi, Diptera: Muscidae) is considered one of the greatest threats to the endemic avifauna of the Galápagos Islands. The fly larvae parasitize nearly every passerine species, including Darwin’s finches. Most P. downsi research to date has focused on the effects of the fly on avian host fitness and mitigation methods. A lag in research related to the genetics of this invasion demonstrates, in part, the need to develop full-scale genomic resources with which to address further questions within this system. In this study, an adult female P. downsi was sequenced to generate a high-quality genome assembly. We examined various features of the genome (e.g., coding regions, non-coding transposable elements) and carried out comparative genomics analysis against other dipteran genomes. We identified lists of gene families that are significantly expanding or contracting in P. downsi that are related to insecticide resistance, detoxification, and counter defense against host immune responses. The P. downsi genome assembly provides an important resource for studying the molecular basis of successful invasion in the Galápagos and the dynamics of its population across multiple islands. The findings of significantly changing gene families associated with insecticide resistance and immune responses highlight the need for further investigations into the role of different gene families in aiding the fly’s successful invasion. Furthermore, this genomic resource provides a necessary tool to better inform future research studies and mitigation strategies aimed at minimizing the fly’s impact on Galápagos birds.

Geometry and dynamics link form, function, and evolution of finch beaks

Darwin’s finches are a classic example of adaptive radiation, exemplified by their adaptive and functional beak morphologies. To quantify their form, we carry out a morphometric analysis of the three-dimensional beak shapes of all of Darwin’s finches and find that they can be fit by a transverse parabolic shape with a curvature that increases linearly from the base toward the tip of the beak. The morphological variation of beak orientation, aspect ratios, and curvatures allows us to quantify beak function in terms of the elementary theory of machines, consistent with the dietary variations across finches. Finally, to explain the origin of the evolutionary morphometry and the developmental morphogenesis of the finch beak, we propose an experimentally motivated growth law at the cellular level that simplifies to a variant of curvature-driven flow at the tissue level and captures the range of observed beak shapes in terms of a simple morphospace. Altogether, our study illuminates how a minimal combination of geometry and dynamics allows for functional form to develop and evolve.

Darwin's finches - an adaptive radiation constructed from ancestral genetic modules

Recent adaptive radiations are models for investigating mechanisms contributing to the evolution of biodiversity. An unresolved question is the relative importance of new mutations, ancestral variants, and introgressive hybridization for phenotypic evolution and speciation. Here we address this issue using Darwin's finches, which vary in size from an 8g warbler finch with a pointed beak to a 40g large ground finch with a massive blunt beak. We present a highly contiguous genome assembly for one of the species and investigate the genomic architecture underlying phenotypic diversity in the entire radiation. Admixture mapping for beak and body size in the small, medium and large ground finches revealed 28 loci showing strong genetic differentiation. These loci represent ancestral haplotype blocks with origins as old as the Darwin's finch phylogeny (1-2 million years). Genes expressed in the developing beak are overrepresented in these genomic regions. Frequencies of allelic variants at the 28 loci covary with phenotypic similarities in body and beak size across the Darwin's finch phylogeny. These ancestral haplotypes constitute genetic modules for selection, and act as key determinants of the exceptional phenotypic diversity of Darwin's finches. Such ancestral haplotype blocks can be critical for how species adapt to environmental variability and change.

Darwin's finches can have taste preferences, but not for human foods

Urbanization is rapidly changing ecological niches. On the Galapagos Islands, Darwin's finches consume human-introduced foods preferentially; however, it remains unclear why. Here we presented pastry with flavour profiles typical of human foods (oily, salty, sweet) to small and medium ground finches to test if latent taste preferences might drive selection of human foods. If human-food flavours were consumed more than a neutral or bitter control at sites with human foods, then we predicted tastes were acquired after experience with human foods; however, if no site-differences were found then this would indicate latent taste preferences. Contrary to both predictions, we found no evidence that human-food flavours were preferred compared to control flavours. Instead, medium ground finches consumed the bitter control pastry most and wiped their beaks more frequently after feeding on oily and sweet pastry (post-ingestion beak wiping can indicate aversions). Small ground finches showed no differences in consumption but wiped their beaks most after feeding on sweet pastry. Our results suggest that unlike many species, medium and small ground finches do not find bitter-tasting food aversive. Furthermore, taste preferences are unlikely to play a major role in Darwin's finches adaptation to the presence of human foods during increased urbanization.

“An Inexplicable Confusion”

While visiting Galápagos, the young Charles Darwin was confused by the similarity of various finches he observed. We now understand that what we see as different finch species are “species before speciation is complete.” The confusion is inherent: many of them remain similar enough to form fertile hybrids. But a robust difference exists between the groups of ground finches and tree finches, raising the question, what prompted the evolution of that clear distinction? The primary habitats for tree finches are tree species of the wonderful Galápagos daisy genus, Scalesia, that dominate the forests of the humid areas of various islands. Did the evolution of daisies into trees influence the evolution of differences between ground and tree finches? For that matter, how did highland trees evolve from lowland shrubby daisies, thus forming the highland habitat for tree finches? Several lines of evidence, including a contemporary interaction analysis of various birds and trees, suggest that the giant daisies of Galápagos and the tree species of Darwin’s finches coevolved.

Isotopic Niche Segregation among Darwin’s Finches on Santa Cruz Island, Galápagos

Darwin’s finches are a classic example of adaptive radiation involving differential use of dietary resources among sympatric species. Here, we apply stable isotope (δ13C, δ15N, and δ2H) analyses of feathers to examine ecological segregation among eight Darwin’s finch species in Santa Cruz Island, Galápagos collected from live birds and museum specimens (1962–2019). We found that δ13C values were higher for the granivorous and herbivorous foraging guilds, and lower for the insectivorous finches. Values of δ15N were similar among foraging guilds but values of δ2H were higher for insectivores, followed by granivores, and lowest for herbivores. The herbivorous guild generally occupied the largest isotopic standard ellipse areas for all isotopic combinations and the insectivorous guild the smallest. Values of δ2H provided better trophic discrimination than those of δ15N possibly due to confounding influences of agricultural inputs of nitrogen. Segregation among guilds was enhanced by portraying guilds in three-dimensional isotope (δ13C, δ15N, and δ2H) space. Values of δ13C and δ15N were higher for feathers of museum specimens than for live birds. We provide evidence that Darwin’s finches on Santa Cruz Island tend to be generalists with overlapping isotopic niches and suggest that dietary overlap may also be more considerable than previously thought.

Sex identification in embryos and adults of Darwin’s finches

Darwin’s finches are an iconic example of adaptive radiation and evolution under natural selection. Comparative genetic studies using embryos of Darwin’s finches have shed light on the possible evolutionary processes underlying the speciation of this clade. Molecular identification of the sex of embryonic samples is important for such studies, where this information often cannot be inferred otherwise. We tested a fast and simple chicken embryo protocol to extract DNA from Darwin’s finch embryos. In addition, we applied minor modifications to two of the previously reported PCR primer sets for CHD1, a gene used for sexing adult passerine birds. The sex of all 29 tested embryos of six species of Darwin’s finches was determined successfully by PCR, using both primer sets. Next to embryos, hatchlings and fledglings are also impossible to distinguish visually. This extends to juveniles of sexually dimorphic species which are yet to moult in adult-like plumage and beak colouration. Furthermore, four species of Darwin’s finches are monomorphic, males and females looking alike. Therefore, sex assessment in the field can be a source of error, especially with respect to juveniles and mature monomorphic birds outside of the mating season. We caught 567 juveniles and adults belonging to six species of Darwin’s finches and only 44% had unambiguous sex-specific morphology. We sexed 363 birds by PCR: individuals sexed based on marginal sex specific morphological traits; and birds which were impossible to classify in the field. PCR revealed that for birds with marginal sex specific traits, sexing in the field produced a 13% error rate. This demonstrates that PCR based sexing can improve field studies on Darwin’s finches, especially when individuals with unclear sex-related morphology are involved. The protocols used here provide an easy and reliable way to sex Darwin’s finches throughout ontogeny, from embryos to adults.