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.

Morphological ghosts of introgression in Darwin's finch populations.

Many species of plants, animals, and microorganisms exchange genes well after the point of evolutionary divergence at which taxonomists recognize them as species. Genomes contain signatures of past gene exchange and, in some cases, they reveal a legacy of lineages that no longer exist. But genomic data are not available for many organisms, and particularly problematic for reconstructing and interpreting evolutionary history are communities that have been depleted by extinctions. For these, morphology may substitute for genes, as exemplified by the history of Darwin's finches on the Galápagos islands of Floreana and San Cristóbal. Darwin and companions collected seven specimens of a uniquely large form of Geospiza magnirostris in 1835. The populations became extinct in the next few decades, partly due to destruction of Opuntia cactus by introduced goats, whereas Geospiza fortis has persisted to the present. We used measurements of large samples of G. fortis collected for museums in the period 1891 to 1906 to test for unusually large variances and skewed distributions of beak and body size resulting from introgression. We found strong evidence of hybridization on Floreana but not on San Cristóbal. The skew is in the direction of the absent G. magnirostris We estimate introgression influenced 6% of the frequency distribution that was eroded by selection after G. magnirostris became extinct on these islands. The genetic residuum of an extinct species in an extant one has implications for its future evolution, as well as for a conservation program of reintroductions in extinction-depleted communities.

Beak morphometry and morphogenesis across avian radiations.

Adaptive avian radiations associated with the diversification of bird beaks into a multitude of forms enabling different functions are exemplified by Darwin's finches and Hawaiian honeycreepers. To elucidate the nature of these radiations, we quantified beak shape and skull shape using a variety of geometric measures that allowed us to collapse the variability of beak shape into a minimal set of geometric parameters. Furthermore, we find that just two measures of beak shape-the ratio of the width to length and the normalized sharpening rate (increase in the transverse beak curvature near the tip relative to that at the base of the beak)-are strongly correlated with diet. Finally, by considering how transverse sections to the beak centreline evolve with distance from the tip, we show that a simple geometry-driven growth law termed 'modified mean curvature flow' captures the beak shapes of Darwin's finches and Hawaiian honeycreepers. A surprising consequence of the simple growth law is that beak shapes that are not allowed based on the developmental programme of the beak are also not observed in nature, suggesting a link between evolutionary morphology and development in terms of growth-driven developmental constraints.

Zebra finches (Taeniopygia guttata) demonstrate cognitive flexibility in using phonology and sequence of syllables in auditory discrimination.

Zebra finches rely mainly on syllable phonology rather than on syllable sequence when they discriminate between two songs. However, they can also learn to discriminate two strings containing the same set of syllables by their sequence. How learning about the phonological characteristics of syllables and their sequence relate to each other and to the composition of the stimuli is still an open question. We compared whether and how the zebra finches' relative sensitivity for syllable phonology and syllable sequence depends on the differences between syllable strings. Two groups of zebra finches were trained in a Go-Left/Go-Right task to discriminate either between two strings in which each string contained a unique set of song syllables ('Different-syllables group') or two strings in which both strings contained the same set of syllables, but in a different sequential order ('Same-syllables group'). We assessed to what extent the birds in the two experimental groups attend to the spectral characteristics and the sequence of the syllables by measuring the responses to test strings consisting of spectral modifications or sequence changes. Our results showed no difference in the number of trials needed to discriminate strings consisting of either different or identical sets of syllables. Both experimental groups attended to changes in spectral features in a similar way, but the group for which both training strings consisted of the same set of syllables responded more strongly to changes in sequence than the group for which the training strings consisted of different sets of syllables. This outcome suggests the presence of an additional learning process to learn about syllable sequence when learning about syllable phonology is not sufficient to discriminate two strings. Our study thus demonstrates that the relative importance of syllable phonology and sequence depends on how these features vary among stimuli. This indicates cognitive flexibility in the acoustic features that songbirds might use in their song recognition.

Do sex differences in construction behavior relate to differences in physical cognitive abilities?

Nest-building behaviour in birds may be particularly relevant to investigating the evolution of physical cognition, as nest building engages cognitive mechanisms for the use and manipulation of materials. We hypothesized that nest-building ecology may be related to physical cognitive abilities. To test our hypothesis, we used zebra finches, which have sex-differentiated roles in nest building. We tested 16 male and 16 female zebra finches on three discrimination tasks in the following order: length discrimination, flexibility discrimination, and color discrimination, using different types of string. We predicted that male zebra finches, which select and deposit the majority of nesting material and are the primary nest builders in this species, would learn to discriminate string length and flexibility-structural traits relevant to nest building-in fewer trials compared to females, but that the sexes would learn color discrimination (not structurally relevant to nest building) in a similar number of trials. Contrary to these predictions, male and female zebra finches did not differ in their speed to learn any of the three tasks. There was, however, consistent among-individual variation in performance: learning speed was positively correlated across the tasks. Our findings suggest that male and female zebra finches either (1) do not differ in their physical cognitive abilities, or (2) any cognitive sex differences in zebra finches are more specific to tasks more closely associated with nest building. Our experiment is the first to examine the potential evolutionary relationship between nest building and physical cognitive abilities.

Among-individual differences in auditory and physical cognitive abilities in zebra finches.

Among-individual variation in performance on cognitive tasks is ubiquitous across species that have been examined, and understanding the evolution of cognitive abilities requires investigating among-individual variation because natural selection acts on individual differences. However, relatively little is known about the extent to which individual differences in cognition are determined by domain-specific compared with domain-general cognitive abilities. We examined individual differences in learning speed of zebra finches across seven different tasks to determine the extent of domain-specific versus domain-general learning abilities, as well as the relationship between learning speed and learning generalization. Thirty-two zebra finches completed a foraging board experiment that included visual and structural discriminations, and then these same birds went through an acoustic operant discrimination experiment that required discriminating between different natural categories of acoustic stimuli. We found evidence of domain-general learning abilities as birds' relative performance on the seven learning tasks was weakly repeatable and a principal components analysis found a first principal component that explained 36% of the variance in performance across tasks with all tasks loading unidirectionally on this component. However, the few significant correlations between tasks and high repeatability within each experiment suggest the potential for domain-specific abilities. Learning speed did not influence an individual's ability to generalize learning. These results suggest that zebra finch performance across visual, structural, and auditory learning relies upon some common mechanism; some might call this evidence of "general intelligence"(g), but it is also possible that this finding is due to other noncognitive mechanisms such as motivation.

Hybridization increases population variation during adaptive radiation.

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.

Foraging zebra finches (Taeniopygia guttata) are public information users rather than conformists.

Social learning enables adaptive information acquisition provided that it is not random but selective. To understand species typical decision-making and to trace the evolutionary origins of social learning, the heuristics social learners use need to be identified. Here, we experimentally tested the nature of majority influence in the zebra finch. Subjects simultaneously observed two demonstrator groups differing in relative and absolute numbers (ratios 1 : 2/2 : 4/3 : 3/1 : 5) foraging from two novel food sources (black and white feeders). We find that demonstrator groups influenced observers' feeder choices (social learning), but that zebra finches did not copy the majority of individuals. Instead, observers were influenced by the foraging activity (pecks) of the demonstrators and in an anti-conformist fashion. These results indicate that zebra finches are not conformist, but are public information users.

Timing of infestation influences virulence and parasite success in a dynamic multi-host-parasite interaction between the invasive parasite, Philornis downsi, and Darwin's finches.

Recently commenced host-parasite interactions provide an excellent opportunity to study co-evolutionary processes. Multi-host systems are especially informative because variation in virulence between hosts and temporal changes provides insight into evolutionary dynamics. However, empirical data under natural conditions are scarce. In the present study, we investigated the interaction between Darwin's finches and the invasive fly Philornis downsi whose larvae feed on the blood of nestlings. Recently, however, the fly has changed its behavior and now also attacks incubating females. Two sympatric hosts are affected differently by the parasite and parasite load has changed over time. Our study observed a reversal of trends described two decades ago: while, currently, small tree finches (Camarhynchus parvulus) experience significantly higher parasite load than warbler finches (Certhidea olivacea), this was the opposite two decades ago. Currently, fledging success is higher in warbler finches compared to small tree finches. Our data indicate that not only intensity but also timing of infestation influences hosts' reproductive success and parasite fitness. During incubation, prevalence was higher in warbler finches, but once chicks had hatched, prevalence was 100% in both species and parasite load was higher in small tree finches. Furthermore, our results suggest faster development and higher reproductive success of P. downsi in small tree finch nests. A change in host preference driven by larvae competition could have led to the reversal in parasite load.

Evidence for rapid downward fecundity selection in an ectoparasite (Philornis downsi) with earlier host mortality in Darwin's finches.

Fecundity selection is a critical component of fitness and a major driver of adaptive evolution. Trade-offs between parasite mortality and host resources are likely to impose a selection pressure on parasite fecundity, but this is little studied in natural systems. The 'fecundity advantage hypothesis' predicts female-biased sexual size dimorphism whereby larger females produce more offspring. Parasitic insects are useful for exploring the interplay between host resource availability and parasite fecundity, because female body size is a reliable proxy for fecundity in insects. Here we explore temporal changes in body size in the myiasis-causing parasite Philornis downsi (Diptera: Muscidae) on the Galápagos Islands under conditions of earlier in-nest host mortality. We aim to investigate the effects of decreasing host resources on parasite body size and fecundity. Across a 12-year period, we observed a mean of c. 17% P. downsi mortality in host nests with 55 ± 6.2% host mortality and a trend of c. 66% higher host mortality throughout the study period. Using specimens from 116 Darwin's finch nests (Passeriformes: Thraupidae) and 114 traps, we found that over time, P. downsi pupae mass decreased by c. 32%, and male (c. 6%) and female adult size (c. 11%) decreased. Notably, females had c. 26% smaller abdomens in later years, and female abdomen size was correlated with number of eggs. Our findings imply natural selection for faster P. downsi pupation and consequently smaller body size and lower parasite fecundity in this newly evolving host-parasite system.

Artificial Light at Night Increases Recruitment of New Neurons and Differentially Affects Various Brain Regions in Female Zebra Finches.

Despite growing evidence that demonstrate adverse effects of artificial light at night (ALAN) on many species, relatively little is known regarding its effects on brain plasticity in birds. We recently showed that although ALAN increases cell proliferation in brains of birds, neuronal densities in two brain regions decreased, indicating neuronal death, which might be due to mortality of newly produced neurons or of existing ones. Therefore, in the present study we studied the effect of long-term ALAN on the recruitment of newborn neurons into their target regions in the brain. Accordingly, we exposed zebra finches (Taeniopygia guttata) to 5 lux ALAN, and analysed new neuronal recruitment and total neuronal densities in several brain regions. We found that ALAN increased neuronal recruitment, possibly as a compensatory response to ALAN-induced neuronal death, and/or due to increased nocturnal locomotor activity caused by sleep disruption. Moreover, ALAN also had a differential temporal effect on neuronal densities, because hippocampus was more sensitive to ALAN and its neuronal densities were more affected than in other brain regions. Nocturnal melatonin levels under ALAN were significantly lower compared to controls, indicating that very low ALAN intensities suppress melatonin not only in nocturnal, but also in diurnal species.

Temporally varying disruptive selection in the medium ground finch (Geospiza fortis).

Disruptive natural selection within populations exploiting different resources is considered to be a major driver of adaptive radiation and the production of biodiversity. Fitness functions, which describe the relationships between trait variation and fitness, can help to illuminate how this disruptive selection leads to population differentiation. However, a single fitness function represents only a particular selection regime over a single specified time period (often a single season or a year), and therefore might not capture longer-term dynamics. Here, we build a series of annual fitness functions that quantify the relationships between phenotype and apparent survival. These functions are based on a 9-year mark-recapture dataset of over 600 medium ground finches (Geospiza fortis) within a population bimodal for beak size. We then relate changes in the shape of these functions to climate variables. We find that disruptive selection between small and large beak morphotypes, as reported previously for 2 years, is present throughout the study period, but that the intensity of this selection varies in association with the harshness of environment. In particular, we find that disruptive selection was strongest when precipitation was high during the dry season of the previous year. Our results shed light on climatic factors associated with disruptive selection in Darwin's finches, and highlight the role of temporally varying fitness functions in modulating the extent of population differentiation.

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.

NOVEL POXVIRAL INFECTION IN THREE FINCH SPECIES ILLEGALLY IMPORTED INTO TRINIDAD, WEST INDIES, WITH IMPLICATIONS FOR NATIVE BIRDS.

Oryzoborus angolensis (Lesser Seed-Finch), Oryzoborus crassirostris (Large-billed Seed-Finch), and Sporophila intermedia (Grey Seedeater) are finch species native to the Caribbean island of Trinidad. These species are locally trapped and kept for their song, but with declining native populations, enthusiasts have turned to illegally importing birds from the South American mainland. The smuggling of wild birds from South America poses significant disease risks to the native bird species of Trinidad. Herein we describe the first case of poxviral infection in these illegally imported birds in Trinidad and partial genome sequence of the causative agent. Phylogenetic analysis of the 4b core protein sequence indicated that the avian poxvirus identified was most closely related to a 2012 avian pox sequence from Brazil, with 96.2% and 98.1% identity at the nucleotide and amino acid level.

Method for improving the quality of genomic DNA obtained from minute quantities of tissue and blood samples using Chelex 100 resin.

BACKGROUND: Although genomic DNA isolation using the Chelex 100 resin is rapid and inexpensive, the DNA obtained by this method has a low concentration in solution and contains suspended impurities. The presence of debris in the DNA solution may result in degradation of DNA on long term storage and inhibition of the polymerase chain reaction. In order to remove impurities and concentrate the DNA in solution, we have introduced modifications in the existing DNA isolation protocol using Chelex-100. We used ammonium acetate to precipitate proteins and a sodium acetate- isopropanol mixture to pellet out DNA which was washed with ethanol. RESULTS: A pure DNA pellet that can be dissolved in water or Tris-EDTA buffer and stored for a long time at - 80 °C was obtained. We also observed a 20-fold change in the DNA concentration following precipitation and re-dissolution. CONCLUSION: Our method is different from other extraction methods since it uses non-toxic, easily available and inexpensive reagents as well as minimal amounts of blood or tissue samples for the DNA extraction process. Besides its use in sex determination and genotyping in lab animals as described in this paper, it may also have applications in forensic science and diagnostics such as the easy detection of pathogenic DNA in blood.

Quantitative host resistance drives the evolution of increased virulence in an emerging pathogen.

Emergent infectious diseases can have a devastating impact on host populations. The high selective pressures on both the hosts and the pathogens frequently lead to rapid adaptations not only in pathogen virulence but also host resistance following an initial outbreak. However, it is often unclear whether hosts will evolve to avoid infection-associated fitness costs by preventing the establishment of infection (here referred to as qualitative resistance) or by limiting its deleterious effects through immune functioning (here referred to as quantitative resistance). Equally, the evolutionary repercussions these different resistance mechanisms have for the pathogen are often unknown. Here, we investigate the co-evolutionary dynamics of pathogen virulence and host resistance following the epizootic outbreak of the highly pathogenic bacterium Mycoplasma gallisepticum in North American house finches (Haemorhous mexicanus). Using an evolutionary modelling approach and with a specific emphasis on the evolved resistance trait, we demonstrate that the rapid increase in the frequency of resistant birds following the outbreak is indicative of strong selection pressure to reduce infection-associated mortality. This, in turn, created the ecological conditions that selected for increased bacterial virulence. Our results thus suggest that quantitative host resistance was the key factor underlying the evolutionary interactions in this natural host-pathogen system.

Timing matters: traffic noise accelerates telomere loss rate differently across developmental stages.

BACKGROUND: Noise pollution is one of the leading environmental health risks for humans, linked to a myriad of stress-related health problems. Yet little is known about the long-term effects of noise on the health and fitness of wildlife. We experimentally investigated the direct and cross-generational effects of traffic noise on telomeres; a measure of cellular ageing that is predictive of disease and longevity in humans and other organisms. We exposed zebra finches (Taenopygia guttata) to three different treatment groups: 1) parents were exposed to traffic noise before and during breeding, together with their nestling young, 2) fledged juveniles but not their parents were exposed to traffic noise, and 3) control group birds were never exposed to traffic noise. RESULTS: Although there was no significant effect of traffic noise exposure at early (pre-fledging) stages of offspring telomere length or loss rate, traffic noise exposure accelerated telomere loss in older (post-fledging) juveniles. CONCLUSIONS: The age-dependent differences found in this study in telomere loss could occur if parents buffer younger offspring against the detrimental effects of noise exposure and/or if younger offspring are less sensitive to noise exposure. Telomere length during early life has been shown to be positively related to lifespan and the observed noise-induced increase of telomere attrition rate could reduce the fitness of the affected birds and potentially alter the population dynamics of birds in noise polluted areas. Our data highlight the need to consider the developmental stage of an organism to better understand the ecological consequences of anthropogenic change.

Individual- and Species-Specific Skin Microbiomes in Three Different Estrildid Finch Species Revealed by 16S Amplicon Sequencing.

An animals' body is densely populated with bacteria. Although a large number of investigations on physiological microbial colonisation have emerged in recent years, our understanding of the composition, ecology and function of the microbiota remains incomplete. Here, we investigated whether songbirds have an individual-specific skin microbiome that is similar across different body regions. We collected skin microbe samples from three different bird species (Taeniopygia gutatta, Lonchura striata domestica and Stagonopleura gutatta) at two body locations (neck region, preen gland area). To characterise the skin microbes and compare the bacterial composition, we used high-throughput 16S rRNA amplicon sequencing. This method proved suitable for identifying the skin microbiome of birds, even though the bacterial load on the skin appeared to be relatively low. We found that across all species, the two evaluated skin areas of each individual harboured very similar microbial communities, indicative of an individual-specific skin microbiome. Despite experiencing the same environmental conditions and consuming the same diet, significant differences in the skin microbe composition were identified among the three species. The bird species differed both quantitatively and qualitatively regarding the observed bacterial taxa. Although each species harboured its own unique set of skin microbes, we identified a core skin microbiome among the studied species. As microbes are known to influence the host's body odour, our findings of an individual-specific skin microbiome might suggest that the skin microbiome in birds is involved in the odour production and could encode information on the host's genotype.

Baseline and stress-induced blood properties of male and female Darwin's small ground finch (Geospiza fuliginosa) of the Galapagos Islands.

Birds are renowned for exhibiting marked sex-specific differences in activity levels and reproductive investment during the breeding season, potentially impacting circulating blood parameters associated with stress and energetics. Males of many passerines often do not incubate, but they experience direct exposure to intruder threat and exhibit aggressive behaviour during the nesting phase in order to defend territories against competing males and predators. Nesting females often have long bouts of inactivity during incubation, but they must remain vigilant of the risks posed by predators and conspecific intruders approaching the nest. Here, we use 33 free-living male (n = 16) and female (n = 17) Darwin's small ground finches (Geospiza fuliginosa) on Floreana Island (Galapagos Archipelago) to better understand how sex-specific roles during the reproductive period impact baseline and stress-induced levels of plasma corticosterone (CORT), blood glucose and haematocrit. Specifically, we hypothesise that males are characterised by higher baseline values given their direct and relatively frequent exposure to intruder threat, but that a standardised stress event (capture and holding) overrides any sex-specific differences. In contrast with expectations, baseline levels of all blood parameters were similar between sexes (13.4 ±â€¯1.9 ng ml-1 for CORT, 13.7 ±â€¯0.4 mmol l-1 for glucose, 58.3 ±â€¯0.8% for haematocrit). Interestingly, females with higher body condition had lower baseline haematocrit. All blood parameters changed with time since capture (range 1.2-41.3 min) in both sexes, whereby CORT increased linearly, haematocrit decreased linearly, and glucose increased to a peak at ∼20 min post-capture and declined to baseline levels thereafter. Our results do not support the hypothesis that sex-specific roles during the reproductive period translate to differences in blood parameters associated with stress and energetics, but we found some evidence that blood oxygen transport capacity may decline as finches increase in body condition.

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.