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.     

Effects of the introduced ectoparasite Philornis downsi on haemoglobin level and nestling survival in Darwin's Small Ground Finch (Geospiza fuliginosa)

Abstract: The physiological impacts and fitness costs of parasitism by an introduced ectoparasitic fly, Philornis downsi (Muscidae), were studied in nestlings of Darwin's Small Ground Finch, Geospiza fuliginosa (Geospizinae), on the Galápagos Archipelago. Whole blood haemoglobin (Hb) concentration was used to measure host response to ectoparasitism due to its high repeatability and validity, as well as for its key role in aerobic activities that affect fitness, such as flight capacity and nestling begging intensity. Increased numbers of ectoparasitic larvae of P. downsi were strongly correlated with lower Hb levels in nestlings in the absence of blood parasites. Furthermore, immature red blood cell counts were negatively correlated with Hb level and positively correlated with P. downsi intensity. Nestlings with high levels of parasitism suffered higher mortality, which varied with clutch size. Our results provide evidence that endemic Galápagos bird populations are physiologically compromised by P. downsi and experience substantial fitness costs due to ectoparasitism.     

Isolation, characterization and multiplex polymerase chain reaction of novel microsatellite loci for the avian parasite Philornis downsi (Diptera: Muscidae)

An enrichment technique was used to isolate 11 di-, tri-, and tetra microsatellites for the parasitic fly Philornis downsi (Diptera: Muscidae). These loci were polymerase chain reaction amplified in singleplexes or two-plexes for P. downsi. The loci showed low to moderate polymorphism, exhibited between three and four alleles, and observed heterozygosity ranged from 0.05 to 0.86. These new markers will be useful for population-level and paternity analyses and will provide valuable information about the ecology of this high-impact parasite of vulnerable bird species.     

Population Response of Giant Galápagos Tortoises to Feral Goat Removal

Efforts to eradicate nonnative mammals to restore oceanic island ecosystems have become increasingly successful but parallel tracking of response by native species for which control efforts are intended to benefit has been rare. A major campaign to eradicate nonnative goats and burros was initiated in 1995 on Alcedo Volcano in the Galápagos Archipelago that ultimately removed 62,868 goats and eliminated them by 2006. Planners of the eradication program had the foresight to invest in intensive monitoring of the status of the volcano's giant tortoise (Chelonoidis nigra) population whose welfare was a primary motivation for the eradication effort. Monitoring revealed an increase in the proportion of juveniles among all tortoises as well as increased growth rates of individual tortoises on Alcedo Volcano from earlier to later phases of the eradication campaign. Over the same time frame in a control population on nearby Santa Cruz Island (where goats and donkeys were not removed) juvenile fraction and individual growth rates remained unchanged. Although goat removal coincided with occurrence of a rare climatic event that simultaneously boosted forage availability for tortoises, failure to observe a comparable improvement in the control population implies that removal of goats and burros was the primary causative factor of improving population status of tortoises on Alcedo Volcano.     

Isolation and characterization of microsatellite loci from Galápagos lava lizards (Microlophus spp.)

We describe the isolation of microsatellite loci from Galápagos lava lizards (Microlophus spp.) using an enriched genomic library. Twelve loci that are polymorphic among six populations from two species are described. Characterization of these loci in 20 individuals within one population (Isla Plaza Sur) showed seven to be polymorphic with 3–11 alleles. Heterozygosities within this population were high (0.32–0.90) and did not deviate from Hardy–Weinberg expectations. We suggest that these markers will be useful in studies of population differentiation within and among islands across the Galápagos archipelago.     

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.     

Cryptic diversity in Black rats Rattus rattus of the Galápagos Islands,Ecuador

Human activity has facilitated the introduction of a number of alien mammal species to the Galápagos Archipelago. Understanding the phylogeographic history and population genetics of invasive species on the Archipelago is an important step in predicting future spread and designing effective management strategies. In this study, we describe the invasion pathway of Rattus rattus across the Galápagos using microsatellite data, coupled with historical knowledge. Microsatellite genotypes were generated for 581 R. rattus sampled from 15 islands in the archipelago. The genetic data suggest that there are at least three genetic lineages of R. rattus present on the Galápagos Islands. The spatial distributions of these lineages correspond to the main centers of human settlement in the archipelago. There was limited admixture among these three lineages, and these finding coupled with low rates of gene flow among island populations suggests that interisland movement of R. rattus is rare. The low migration among islands recorded for the species will have a positive impact on future eradication efforts.     

Conservation status of landbirds on Floreana: the smallest inhabited Galápagos Island

On Floreana, the smallest inhabited island in the Galápagos, populations of several species of birds have either been extirpated or, based on anecdotal evidence and small‐scale surveys, are declining. Our objective, therefore, was to conduct a comprehensive survey of landbirds encompassing the entire island during three breeding seasons (2014–2016). We conducted surveys at 59 points in 2014, 257 in 2015, and 295 in 2016. Each survey point was sampled once. We detected 12 species during our surveys. Galápagos Flycatchers, Yellow Warblers, Small and Medium ground‐finches, and Small Tree‐Finches were widely distributed over the entire island. Common Cactus‐Finches and Medium Tree‐Finches had more restricted distributions in the lower or higher parts of the island. Few Dark‐billed Cuckoos (Coccyzus melacoryphus), Paint‐billed Crakes (Neocrex erythrops), Galápagos Doves (Zenaida galapagoensis), and Galápagos Short‐eared Owls (Asio flammeus galapagoensis) were recorded. Small Ground‐Finches and Small Tree‐Finches were found at densities comparable to those on other Galápagos Islands, whereas densities of Galápagos Flycatchers and Yellow Warblers were higher on Floreana than on other islands. Endemic Medium Tree‐Finches were confined to an area of 24 km², mainly in the highlands, but were still widespread and common in their restricted habitat, with the number of territories estimated to be between 3900 and 4700. Of 22 originally occurring landbirds on Floreana, no fewer than 10 species have either been extirpated or are likely to have been extirpated since the arrival of the first human inhabitants. The combined effects of introduced mammals, large‐scale habitat destruction, and direct human persecution were responsible for the extirpation of six species during the 19th century. Three additional species have been extirpated since 1960, likely due to the introduction of the parasitic fly Philornis downsi, and this fly remains a major threat for the remaining bird species. Developing strategies for reducing the impact of these flies on the birds of the Galapagos Islands must be a high priority. In addition, habitat management and restoration, including the control of invasive plants and promotion of native tree species, will be critically important in conserving landbird populations on Floreana.     

The vector ecology of introduced Culex quinquefasciatus populations,and implications for future risk of West Nile virus emergence in the Galápagos archipelago

Culex quinquefasciatus Say (Diptera: Culicidae), an important vector of West Nile virus (WNV) in the U.S.A., was first detected on the Galápagos Islands (Ecuador) in the 1980s. However, little is known of its ecology, distribution or capacity for arbovirus transmission in the Galápagos. We characterize details of lifecycle (including gonotrophic period), temporal abundance, spatial distribution, vector competence and host‐feeding behaviour. Culex quinquefasciatus was detected on five islands of the Galápagos during 2006–2011. A period of 7–14 days was required for egg–adult emergence; water salinity above 5 ppt was demonstrated to hinder larval development. Blood‐meal analysis indicated feeding on reptiles, birds and mammals. Assessment of WNV vector competency of Galápagos C. quinquefasciatus showed a median infectious dose of 7.41 log₁₀ plaque‐forming units per millilitre and evidence of vertical transmission (minimal filial infection rate of 3.7 per 1000 progeny). The distribution of C. quinquefasciatus across the archipelago could be limited by salt intolerance, and its abundance constrained by high temperatures. Feeding behaviour indicates potential to act as a bridge vector for transmission of pathogens across multiple taxa. Vertical transmission is a potential persistence mechanism for WNV on Galápagos. Together, our results can be used for epidemiological assessments of WNV and target vector control, should this pathogen reach the Galápagos Islands.     

Isolation and characterization of microsatellite loci in the Galápagos Opuntia weevil Gerstaeckeria galapagoensis (Coleoptera,Curculionidae)

Five microsatellite loci were isolated from the Galápagos weevil Gerstaeckeria galapagoensis. Polymorphism ranged from two to seven alleles, and observed and expected heterozygosities ranged from 0.286 to 0.917 and 0.254 to 0.683, respectively.     

Isolation and characterization of microsatellite loci in Galápagos caterpillar hunters (Coleoptera,Carabidae, Calosoma)

Five microsatellite loci were isolated from the Galápagos caterpillar hunter Calosoma granatense. Polymorphism ranges from four to 14 alleles, and observed and expected heterozygosities range from 0.138 to 0.889 and 0.197–0.902, respectively. Cross‐amplification of the developed primers was successful in the related species C. leleuporum.     

Development of primers to characterize the mitochondrial control region of Galápagos land and marine iguanas (Conolophus and Amblyrhynchus)

Primers were developed for the amplification and sequencing of the mitochondrial control region of Galápagos land (Conolophus) and marine (Amblyrhynchus) iguanas. Sequences were obtained for four land iguana samples from two islands and for 28 marine iguana samples from three islands. A series of 70–80 bp tandem repeats adjacent to the control region are described and preliminary quantification of intra‐ and interspecific sequence divergence is included.     

A set of highly discriminating microsatellite loci for the Galápagos marine iguana Amblyrhynchus cristatus

We describe here the cloning of 12 (7 dinucleotide, 1 trinucleotide and 4 tetranucleotide) microsatellite loci for the Galápagos marine iguana Amblyrhynchus cristatus. When tested for individuals from five different island populations on the Galápagos archipelago, high genetic diversities (9–20 alleles per locus) and heterozygosities (0.200–0.944) were observed. All loci showed no obvious deviations from Hardy–Weinberg equilibrium. The new set of microsatellite loci was able to assign individuals reliably to their island of origin, thus being able to discriminate between residents and migrants between islands.     

Genetic and morphometric evidence on a Galápagos Island exposes founder effects and diversification in the first‐known (truly) feral western dog population

Domesticated animals that revert to a wild state can become invasive and significantly impact native biodiversity. Although dogs can be problematic locally, only the Australasian dingo is known to occur in isolation from humans. Western dogs have experienced more intense artificial selection, which potentially limits their invasiveness. However, feral dogs eradicated from Isabela Island, Galápagos in the 1980s could be the first‐known exception. We used DNA and morphometric data from 92 of these dogs to test the hypotheses that (i) these dogs persisted independently of humans for up to a century and a half since descending from a handful of dogs introduced in the early 1800s, vs. (ii) similarly to other western feral dog populations, they reflected continuous recruitment of strays from human settlements on a portion of the Island. We detected one dominant maternal lineage and one dominant paternal lineage shared by the three subpopulations, along with low autosomal genetic diversity, consistent with the hypothesized common origins from a small founder population. Genetic diversity patterns among the three island subpopulations were consistent with stepping‐stone founder effects, while morphometric differentiation suggested rapid phenotypic divergence, possibly due to drift and reinforced by selection corresponding to distinct microclimates and habitats on Isabela. Despite the continued presence of free‐ranging dogs in the vicinity of settlements on Isabela and other Galápagos Islands, feral populations have not reestablished in remote areas since the 1980s, emphasizing the rarity of conditions necessary for feralization of modern western dogs.     

Habitat filtering not dispersal limitation shapes oceanic island floras: species assembly of the Galápagos archipelago

Remote locations, such as oceanic islands, typically harbour relatively few species, some of which go on to generate endemic radiations. Species colonising these locations tend to be a non‐random subset from source communities, which is thought to reflect dispersal limitation. However, non‐random colonisation could also result from habitat filtering, whereby only a few continental species can become established. We evaluate the imprints of these processes on the Galápagos flora by analysing a comprehensive regional phylogeny for ~ 39 000 species alongside information on dispersal strategies and climatic suitability. We found that habitat filtering was more important than dispersal limitation in determining species composition. This finding may help explain why adaptive radiation is common on oceanic archipelagoes – because colonising species can be relatively poor dispersers with specific niche requirements. We suggest that the standard assumption that plant communities in remote locations are primarily shaped by dispersal limitation deserves reconsideration.     

Persistence of song types in Darwin's finches,Geospiza fortis,over four decades

Learned bird songs evolve via cultural evolution, with song patterns transmitted across generations by imitative learning. In Darwin''s finches of the Galápagos Islands, males learn songs from their fathers, and song types can be maintained across multiple generations. However, little is known about the time frame over which specific song types are preserved, in the face of copy errors and corresponding modifications to song structure. Here we investigate cultural evolution in songs of male Geospiza fortis, at Academy Bay, Santa Cruz Island, comparing songs recorded in 1961 by R. Bowman (20 individuals) to those recorded in 1999 by J. Podos (16 individuals). For each individual, we characterized four timing and six frequency parameters, and assessed inter-individual variation in song structure using multivariate analysis. Several 1961 song types persisted into 1999, some with remarkable fidelity. Variation among song types was extensive during both years, and we detected no changes in 10 vocal parameters across the sampling period. These results illustrate temporal continuity in a culturally acquired trait, and raise questions about mechanisms that promote stability in song structure.