RESUMO
Humans exert dramatic influences upon the environment, creating novel selective pressures to which organisms must adapt. On the Galapagos, humans have established a permanent presence and have altered selective pressures through influences such as invasive predators and urbanization, affecting iconic species such as Darwin's finches. Here, I ask two key questions: (a) Does antipredator behaviour (e.g., flight initiation distance - FID) change depending on whether invasive predators are historically absent, present, or eradicated? and (b) To what degree does urbanization affect antipredator behaviour? This study is one of the first to quantify antipredator behaviour in endemic species after the eradication of invasive predators. This will help to understand the consequences of invasive predator eradication and inform conservation measures. I quantified FID, an antipredator behaviour, in the small ground finch, across multiple islands in the Galapagos that varied in the presence, absence, or successful eradication of invasive predators. On islands with human populations, I quantified FID in urban and non-urban populations of finches. FID was higher on islands with invasive predators compared to islands with no predators. On islands from which invasive predators were eradicated ~11 years previously, FID was also higher than on islands with no invasive predators. Within islands that had both urban and non-urban populations of finches, FID was lower in urban finch populations, but only above a threshold human population size. FID in larger urban areas on islands with invasive predators was similar to or lower than FID on islands with no history of invasive predators. Overall, these results suggest that invasive predators can have a lasting effect on antipredator behaviour, even after eradication. Furthermore, the effect of urbanization can strongly oppose the effect of invasive predators, reducing antipredator behaviour to levels lower than found on pristine islands with no human influences. These results improve our understanding of human influences on antipredator behaviour which can help inform future conservation and management efforts on islands.
Los humanos pueden ejercer influencias drásticas sobre el medio ambiente creando nuevas presiones selectivas a las cuales los organismos deben adaptarse. En las islas Galápagos, la presencia permanente de humanos ha alterado dichas presiones selectivas modificando factores como la introducción de depredadores y los niveles de urbanización, los mismos que podrían estar afectando a especies icónicas como lo son los pinzones de Darwin. En el presente estudio se planearon dos preguntas claves: (i) ¿el comportamiento anti-depredatorio (ej. la distancia inicial de fuga - DIF) de los pinzones varia entre sitios con presencia, ausencia histórica o erradicación de depredadores introducidos? y (ii) ¿en qué grado la urbanización afecta el comportamiento anti-depredatorio de los pinzones? Este estudio es uno de los primeros en cuantificar el comportamiento anti-depredatorio en especies endémicas después de la erradicación de depredadores invasivos, lo cual permite entender las consecuencias que pueden tener los mismos en los ecosistemas, y del mismo modo provee información valiosa para el desarrollo de medidas de conservación. Yo cuantifiqué la distancia inicial de fuga (DIF), que es un comportamiento anti-depredatorio en los pinzones de Darwin a lo largo de diferentes islas en Galápagos con presencia, ausencia y erradicación exitosa de depredadores introducidos. En islas con poblaciones humanas, comparamos la distancia inicial de fuga entre poblaciones de pinzones que viven cerca o no a zonas urbanas. La distancia inicial de fuga (DIF) de los pinzones fue mayor en las islas con presencia de depredadores introducidos en comparación con las islas en los que éstos están ausentes. Adicionalmente, en islas donde los depredadores introducidos fueron erradicados aproximadamente hace 11 años, la distancia inicial de fuga en los pinzones fue también mayor en comparación con las islas donde hay ausencia de depredadores. En las islas con poblaciones de pinzones cercanas o no a zonas urbanas, la distancia inicial de fuga fue mayor en los pinzones que viven cerca a zonas urbanas, pero solo hasta cierto límite de tamaño de población humana. Finalmente, la distancia inicial de fuga de los pinzones en áreas urbanas grandes con presencia de depredadores introducidos fue similar o menor a la distancia inicial de fuga de los pinzones en islas con ausencia histórica de depredadores introducidos. En resumen, los resultados sugieren que los depredadores introducidos pueden tener un efecto duradero en el comportamiento anti-depredatorio de los pinzones, incluso después de haber sido erradicados. Adicionalmente, el impacto de la urbanización puede tener un fuerte efecto opuesto al esperado por la presencia de depredadores introducidos, reduciendo el comportamiento anti-depredatorio de los pinzones a niveles más bajos de lo que se encuentran en islas prístinas sin presencia de influencia humana. Estos resultados nos permiten incrementar la información disponible acerca del impacto antropogénico en el comportamiento anti-depredatorio de especies endémicas, lo cual contribuirá con información relevante para el desarrollo de programas de conservación futuros y planes de manejo de especies introducidas en las islas.
Assuntos
Tentilhões , Passeriformes , Animais , Equador , Humanos , IlhasRESUMO
BACKGROUND: Darwin's finches are a clade of 19 species of passerine birds native to the Galápagos Islands, whose biogeography, specialized beak morphologies, and dietary choices-ranging from seeds to blood-make them a classic example of adaptive radiation. While these iconic birds have been intensely studied, the composition of their gut microbiome and the factors influencing it, including host species, diet, and biogeography, has not yet been explored. RESULTS: We characterized the microbial community associated with 12 species of Darwin's finches using high-throughput 16S rRNA sequencing of fecal samples from 114 individuals across nine islands, including the unusual blood-feeding vampire finch (Geospiza septentrionalis) from Darwin and Wolf Islands. The phylum-level core gut microbiome for Darwin's finches included the Firmicutes, Gammaproteobacteria, and Actinobacteria, with members of the Bacteroidetes at conspicuously low abundance. The gut microbiome was surprisingly well conserved across the diversity of finch species, with one exception-the vampire finch-which harbored bacteria that were either absent or extremely rare in other finches, including Fusobacterium, Cetobacterium, Ureaplasma, Mucispirillum, Campylobacter, and various members of the Clostridia-bacteria known from the guts of carnivorous birds and reptiles. Complementary stable isotope analysis of feathers revealed exceptionally high δ15N isotope values in the vampire finch, resembling top marine predators. The Galápagos archipelago is also known for extreme wet and dry seasons, and we observed a significant seasonal shift in the gut microbial community of five additional finch species sampled during both seasons. CONCLUSIONS: This study demonstrates the overall conservatism of the finch gut microbiome over short (< 1 Ma) divergence timescales, except in the most extreme case of dietary specialization, and elevates the evolutionary importance of seasonal shifts in driving not only species adaptation, but also gut microbiome composition.
Assuntos
Bactérias/isolamento & purificação , Tentilhões/microbiologia , Microbioma Gastrointestinal , Animais , Bactérias/classificação , Bactérias/genética , Evolução Biológica , Clima , DNA Bacteriano/genética , Equador , Fezes/microbiologia , Tentilhões/classificação , Tentilhões/genética , Trato Gastrointestinal/microbiologia , Filogenia , RNA Ribossômico 16S/genética , Estações do AnoRESUMO
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 (nâ¯=â¯16) and female (nâ¯=â¯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¯1.9â¯ngâ¯ml-1 for CORT, 13.7⯱â¯0.4â¯mmolâ¯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 1.2-41.3â¯min) in both sexes, whereby CORT increased linearly, haematocrit decreased linearly, and glucose increased to a peak at â¼20â¯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.
Assuntos
Corticosterona/sangue , Tentilhões/crescimento & desenvolvimento , Animais , Equador , Feminino , MasculinoRESUMO
BACKGROUND: The molecular basis of evolutionary change is assumed to be genetic variation. However, growing evidence suggests that epigenetic mechanisms, such as DNA methylation, may also be involved in rapid adaptation to new environments. An important first step in evaluating this hypothesis is to test for the presence of epigenetic variation between natural populations living under different environmental conditions. RESULTS: In the current study we explored variation between populations of Darwin's finches, which comprise one of the best-studied examples of adaptive radiation. We tested for morphological, genetic, and epigenetic differences between adjacent "urban" and "rural" populations of each of two species of ground finches, Geospiza fortis and G. fuliginosa, on Santa Cruz Island in the Galápagos. Using data collected from more than 1000 birds, we found significant morphological differences between populations of G. fortis, but not G. fuliginosa. We did not find large size copy number variation (CNV) genetic differences between populations of either species. However, other genetic variants were not investigated. In contrast, we did find dramatic epigenetic differences between the urban and rural populations of both species, based on DNA methylation analysis. We explored genomic features and gene associations of the differentially DNA methylated regions (DMR), as well as their possible functional significance. CONCLUSIONS: In summary, our study documents local population epigenetic variation within each of two species of Darwin's finches.
Assuntos
Cidades , Epigênese Genética , Tentilhões/genética , Variação Genética , Animais , Cromossomos/genética , Ilhas de CpG/genética , Variações do Número de Cópias de DNA/genética , Metilação de DNA/genética , Equador , Geografia , Masculino , Transdução de Sinais/genética , Especificidade da Espécie , Espermatozoides/metabolismoRESUMO
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.
Assuntos
Bico/anatomia & histologia , Tentilhões/genética , Seleção Genética , Adaptação Biológica/genética , Alelos , Animais , Equador , Ligação Genética , Loci Gênicos , Genética Populacional , Hibridização Genética , Ilhas , Desequilíbrio de Ligação , Polimorfismo de Nucleotídeo ÚnicoRESUMO
Introduced parasites threaten native host species that lack effective defenses. Such parasites increase the risk of extinction, particularly in small host populations like those on islands. If some host species are tolerant to introduced parasites, this could amplify the risk of the parasite to vulnerable host species. Recently, the introduced parasitic nest fly Philornis downsi has been implicated in the decline of Darwin's finch populations in the Galápagos Islands. In some years, 100% of finch nests fail due to P. downsi; however, other common host species nesting near Darwin's finches, such as the endemic Galápagos mockingbird (Mimus parvulus), appear to be less affected by P. downsi. We compared effects of P. downsi on mockingbirds and medium ground finches (Geospiza fortis) on Santa Cruz Island in the Galápagos. We experimentally manipulated the abundance of P. downsi in nests of mockingbirds and finches to measure the direct effect of the parasite on the reproductive success of each species of host. We also compared immunological and behavioral responses by each species of host to the fly. Although nests of the two host species had similar parasite densities, flies decreased the fitness of finches but not mockingbirds. Neither host species had a significant antibody-mediated immune response to P. downsi. Moreover, finches showed no significant increase in begging, parental provisioning, or plasma glucose levels in response to the flies. In contrast, parasitized mockingbird nestlings begged more than nonparasitized mockingbird nestlings. Greater begging was correlated with increased parental provisioning behavior, which appeared to compensate for parasite damage. The results of our study suggest that finches are negatively affected by P. downsi because they do not have such behavioral mechanisms for energy compensation. In contrast, mockingbirds are capable of compensation, making them tolerant hosts, and a possible indirect threat to Darwin's finches.
Assuntos
Tentilhões/fisiologia , Passeriformes/fisiologia , Animais , Equador , Monitoramento Ambiental , Tentilhões/parasitologia , Ilhas , Parasitos , Passeriformes/parasitologiaRESUMO
The trajectory of speciation involves geographic isolation of ancestral populations followed by divergence by natural selection, genetic drift or sexual selection. Once started, the process may experience fits and starts, as sometimes diverging populations intermittently reconnect. In theory populations might cycle between stages of differentiation and never attain species status, a process we refer to as Sisyphean evolution. We argue that the six putative ground finch species (genus Geospiza) of the Galápagos Islands represent a dramatic example of Sisyphean evolution that has been confused with the standard model of speciation. The dynamic environment of the Galápagos, closely spaced islands, and frequent dispersal and introgression have prevented the completion of the speciation process. We suggest that morphological clusters represent locally adapted ecomorphs, which might mimic, and have been confused with, species, but these ecomorphs do not form separate gene pools and are ephemeral in space and time. Thus the pattern of morphological, behavioural and genetic variation supports recognition of a single species of Geospiza, which we suggest should be recognized as Darwin's ground finch (Geospiza magnirostris). We argue that instead of providing an icon of insular speciation and adaptive radiation, which is featured in nearly every textbook on evolutionary biology, Darwin's ground finch represents a potentially more interesting phenomenon, one of transient morphs trapped in an unpredictable cycle of Sisyphean evolution. Instead of revealing details of the origin of species, the mechanisms underlying the transient occurrence of ecomorphs provide one of the best illustrations of the antagonistic effects of natural selection and introgression.