Phylogeography of the Galápagos hawk (Buteo galapagoensis): a recent arrival to the Galápagos Islands

Galápagos hawks (Buteo galapagoensis) are one of the most inbred bird species in the world, living in small, isolated island populations. We used mitochondrial sequence and nuclear minisatellite data to describe relationships among Galápagos hawk populations and their colonization history. We sampled 10 populations (encompassing the entire current species range of nine islands and one extirpated population), as well as the Galápagos hawk's closest mainland relative, the Swainson's hawk (B. swainsoni). There was little sequence divergence between Galápagos and Swainson's hawks (only 0.42% over almost 3kb of data), indicating that the hawks colonized Galápagos very recently, likely less than 300,000 years ago, making them the most recent arrivals of the studied taxa. There were only seven, closely related Galápagos hawk haplotypes, with most populations being monomorphic. The mitochondrial and minisatellite data together indicated a general pattern of rapid population expansion followed by genetic isolation of hawk breeding populations. The recent arrival, genetic isolation, and phenotypic differentiation among populations suggest that the Galápagos hawk, a rather new species itself, is in the earliest stages of further divergence.     

Patterns of parasite abundance and distribution in island populations of Galápagos endemic birds

Parasite life-history characteristics, the environment, and host defenses determine variation in parasite population parameters across space and time. Parasite abundance and distribution have received little attention despite their pervasive effects on host populations and community dynamics. We used analyses of variance to estimate the variability of intensity, prevalence, and abundance of 4 species of lice (Insecta: Phthiraptera) infecting Galápagos doves and Galápagos hawks and 1 haemosporidian parasite (Haemosporida: Haemoproteidae) infecting the doves across island populations throughout their entire geographic ranges. Population parameters of parasites with direct life cycles varied less within than among parasite species, and intensity and abundance did not differ significantly across islands. Prevalence explained a proportion of the variance (34%), similar to infection intensity (33%) and parasite abundance (37%). We detected a strong parasite species-by-island interaction, suggesting that parasite population dynamics is independent among islands. Prevalence (up to 100%) and infection intensity (parasitemias up to 12.7%) of Haemoproteus sp. parasites varied little across island populations.     

Disease ecology in the Galápagos Hawk (Buteo galapagoensis): host genetic diversity, parasite load and natural antibodies

An increased susceptibility to disease is one hypothesis explaining how inbreeding hastens extinction in island endemics and threatened species. Experimental studies show that disease resistance declines as inbreeding increases, but data from in situ wildlife systems are scarce. Genetic diversity increases with island size across the entire range of an extremely inbred Galápagos endemic bird, providing the context for a natural experiment examining the effects of inbreeding on disease susceptibility. Extremely inbred populations of Galápagos hawks had higher parasite abundances than relatively outbred populations. We found a significant island effect on constitutively produced natural antibody (NAb) levels and inbred populations generally harboured lower average and less variable NAb levels than relatively outbred populations. Furthermore, NAb levels explained abundance of amblyceran lice, which encounter the host immune system. This is the first study linking inbreeding, innate immunity and parasite load in an endemic, in situ wildlife population and provides a clear framework for assessment of disease risk in a Galápagos endemic.     

Microfilariae in Galápagos penguins (Spheniscus mendiculus) and flightless cormorants (Phalacrocorax harrisi): genetics, morphology, and prevalence

Galapagos penguins (Spheniscus mendiculus) and flightless cormorants (Phalacrocorax harrisi) live in small, isolated populations on the westernmost islands of Isabela and Fernandina in the Galápagos Islands, Ecuador. Between August 2003 and February 2005, 4 field trips, 2 in the cool, dry season (August 2003 and August 2004) and 2 in the hot, rainy season (March 2004 and February 2005), were undertaken; 298 Galápagos penguins and 380 cormorants were sampled for prevalence and intensity of hemoparasites. Microfilariae were found in both the penguins and the cormorants. Blood smears were negative for the presence of other species of hemoparasites. Overall prevalence of microfilariae across seasons was 42.0% in cormorants and 13.8% in the penguins. Intensity of infection was generally low (mean = 3.2-31.7 in 25 fields across seasons and species) with the exception of a few individuals with markedly high intensities of parasites (>300 in 25 fields in 1 cormorant). Prevalence of microfilariae increased significantly over the 4 sampling periods for cormorants, but not for penguins. Prevalences were significantly higher in cormorants than in penguins for 3 of the 4 collecting trips. Male penguins had higher prevalences than females; however, there were no gender differences in cormorants. No relation was detected between body mass and either presence or intensity of parasitism. Morphological characteristics of the microfilariae are also described and specimens from each host species were similar in all characters measured. DNA sequence data from the mitochondrial cytochrome c oxidase subunit I gene were consistent with the morphological evidence and together demonstrate that the penguins and cormorants are likely to be infected with the same species of microfilariae.     

Co-phylogeography and comparative population genetics of the threatened Galápagos hawk and three ectoparasite species: ecology shapes population histories within parasite communities

Comparative microevolutionary studies of multiple parasites occurring on a single host species can help shed light on the processes underlying parasite diversification. We compared the phylogeographical histories, population genetic structures and population divergence times of three co-distributed and phylogenetically independent ectoparasitic insect species, including an amblyceran and an ischnoceran louse (Insecta: Phthiraptera), a hippoboscid fly (Insecta: Diptera) and their endemic avian host in the Galápagos Islands. The Galápagos hawk (Aves: Falconiformes: Buteo galapagoensis) is a recently arrived endemic lineage in the Galápagos Islands and its island populations are diverging evolutionarily. Each parasite species differed in relative dispersal ability and distribution within the host populations, which allowed us to make predictions about their degree of population genetic structure and whether they tracked host gene flow and colonization history among islands. To control for DNA region in comparisons across these phylogenetically distant taxa, we sequenced ~1 kb of homologous mitochondrial DNA from samples collected from all island populations of the host. Remarkably, the host was invariant across mitochondrial regions that were comparatively variable in each of the parasite species, to degrees consistent with differences in their natural histories. Differences in these natural history traits were predictably correlated with the evolutionary trajectories of each parasite species, including rates of interisland gene flow and tracking of hosts by parasites. Congruence between the population structures of the ischnoceran louse and the host suggests that the ischnoceran may yield insight into the cryptic evolutionary history of its endangered host, potentially aiding in its conservation management.     

A hitchhikers guide to the Galápagos: co-phylogeography of Galápagos mockingbirds and their parasites

Background

Parasites are evolutionary hitchhikers whose phylogenies often track the evolutionary history of their hosts. Incongruence in the evolutionary history of closely associated lineages can be explained through a variety of possible events including host switching and host independent speciation. However, in recently diverged lineages stochastic population processes, such as retention of ancestral polymorphism or secondary contact, can also explain discordant genealogies, even in fully co-speciating taxa. The relatively simple biogeographic arrangement of the Galápagos archipelago, compared with mainland biomes, provides a framework to identify stochastic and evolutionary informative components of genealogic data in these recently diverged organisms.

Results

Mitochondrial DNA sequences were obtained for four species of Galápagos mockingbirds and three sympatric species of ectoparasites - two louse and one mite species. These data were complemented with nuclear EF1α sequences in selected samples of parasites and with information from microsatellite loci in the mockingbirds. Mitochondrial sequence data revealed differences in population genetic diversity between all taxa and varying degrees of topological congruence between host and parasite lineages. A very low level of genetic variability and lack of congruence was found in one of the louse parasites, which was excluded from subsequent joint analysis of mitochondrial data. The reconciled multi-species tree obtained from the analysis is congruent with both the nuclear data and the geological history of the islands.

Conclusions

The gene genealogies of Galápagos mockingbirds and two of their ectoparasites show strong phylogeographic correlations, with instances of incongruence mostly explained by ancestral genetic polymorphism. A third parasite genealogy shows low levels of genetic diversity and little evidence of co-phylogeny with their hosts. These differences can mostly be explained by variation in life-history characteristics, primarily host specificity and dispersal capabilities. We show that pooling genetic data from organisms living in close ecological association reveals a more accurate phylogeographic history for these taxa. Our results have implications for the conservation and taxonomy of Galápagos mockingbirds and their parasites.     

Recent colonization of the Galápagos by the tree Geoffroea spinosa Jacq. (Leguminosae)

This study puts together genetic data and an approximate bayesian computation (ABC) approach to infer the time at which the tree Geoffroea spinosa colonized the Galápagos Islands. The genetic diversity and differentiation between Peru and Galápagos population samples, estimated using three chloroplast spacers and six microsatellite loci, reveal significant differences between two mainland regions separated by the Andes mountains (Inter Andean vs. Pacific Coast) as well as a significant genetic differentiation of island populations. Microsatellites identify two distinct geographical clusters, the Galápagos and the mainland, and chloroplast markers show a private haplotype in the Galápagos. The nuclear distinctiveness of the Inter Andean populations suggests current restricted pollen flow, but chloroplast points to cross‐Andean dispersals via seeds, indicating that the Andes might not be an effective biogeographical barrier. The ABC analyses clearly point to the colonization of the Galápagos within the last 160 000 years and possibly as recently as 4750 years ago (475 generations). Founder events associated with colonization of the two islands where the species occurs are detected, with Española having been colonized after Floreana. We discuss two nonmutually exclusive possibilities for the colonization of the Galápagos, recent natural dispersal vs. human introduction.     

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.     

Radiation following long‐distance dispersal: the contributions of time,opportunity and diaspore morphology in Sicyos (Cucurbitaceae)

Aim  To infer the most plausible explanations for the presence of 14 species of the Neotropical cucurbit genus Sicyos on the Hawaiian Islands, two on the Galápagos Islands, two in Australia, and one in New Zealand. Location  Neotropics, the Hawaiian and Galápagos archipelagos, Australia and New Zealand. Methods  We tested long‐problematic generic boundaries in the tribe Sicyoeae and reconstructed the history of Sicyos using plastid and nuclear DNA sequences from 87 species (many with multiple accessions) representing the group’s generic and geographic diversity. Maximum likelihood and Bayesian approaches were used to infer relationships, divergence times, biogeographic history and ancestral traits. Results  Thirteen smaller genera, including Sechium, are embedded in Sicyos, which when re‐circumscribed as a monophyletic group comprises 75 species. The 14 Hawaiian species of Sicyos descended from a single ancestor that arrived c. 3 million years ago (Ma), Galápagos was reached twice at c. 4.5 and 1 Ma, the species in Australia descended from a Neotropical ancestor (c. 2 Ma), and New Zealand was reached from Australia. Time since arrival thus does not correlate with Sicyos species numbers on the two archipelagos. Main conclusions  A plausible mechanism for the four trans‐Pacific dispersal events is adherence to birds of the tiny hard fruit with retrorsely barbed spines found in those lineages that underwent long‐distance migrations. The Hawaiian clade has lost these spines, resulting in a lower dispersal ability compared with the Galápagos and Australian lineages, and perhaps favouring allopatric speciation.     

Eight polymorphic microsatellite markers isolated from the widespread avian louse Colpocephalum turbinatum (Phthiraptera: Amblycera: Menoponidae)

We report eight novel microsatellite loci for Colpocephalum turbinatum, a parasitic louse of the endangered Galápagos hawk (Buteo galapagoensis). Two island populations of C. turbinatum (N = 30) were genotyped for each locus. We found between two and 12 alleles per locus, polymorphic information content from 0.268 to 0.798, observed heterozygosity from 0.067 to 0.667 and no linkage disequilibrium was detected between loci. These markers will be useful in understanding contemporary gene flow of C. turbinatum among islands in the Galápagos and in understanding transmission dynamics between B. galapagoensis hosts, within and between social groups. Because this louse is unusually widespread among avian host taxa, parasitizing at least 53 bird species in the Falconiformes, Strigiformes and Columbiformes, these markers are likely to be useful outside the context of the Galápagos Islands.     

Phoretic association of mites and mallophaga with the pigeon fly Pseudolynchia canariensis

Myialges anchora Trouessart, 1906 and M. lophortyx (Furman & Tarshis, 1953) gravid females, surrounded by clusters of eggs, were found strongly inserted into the cuticle of head, thorax, abdomen, femurs and wings of Pseudolynchia canariensis (Macquart, 1840), a hippoboscid fly parasite of the pigeon. This lousefly results obligatory host for ovigerous females of Myialges and for the development of their eggs, and phoretic host because the dispersal of hatching larvae to new hosts may then occur with dispersal of fly carriers. Together with the Myiolges species, not ovigerous females of Ornithocheyletia hallae Smiley, 1970 and Columbicola columbae (Linnaeus, 1758) were found on the pigeon fly.     

DIATOMS (BACILLARIOPHYTA) OF ISOLATED ISLANDS: NEW TAXA IN THE GENUS NAVICULA SENSU STRICTO FROM THE GALáPAGOS ISLANDS1

The diatoms (Bacillariophyta) from a coastal lagoon from the Diablas wetlands (Isla Isabela, the Galápagos Islands) were studied in material from surface samples and a sediment core spanning the past 2,700 years in order to examine evidence of diatom evolution under geographic isolation. The total number of taxa found was ～100. Ultrastructural variation in valve morphology between members of Galápagos taxa was used to describe 10 species from the genus Navicula sensu stricto, which are new to science. Four taxa: N. isabelensis, N. isabelensoides, N. isabelensiformis, and N. isabelensiminor, shared several key characteristics that may be indicative of a common evolutionary heritage; these species therefore provide possible evidence for the in situ evolution of diatoms in the Galápagos coastal lagoons. Shared morphological characteristics include: (i) stria patterning in the central area, (ii) an elevated and thickened external raphe‐sternum, (iii) external central raphe endings that are slightly deflected toward the valve primary side, and (iv) an arched valve surface. To explain these findings, two models were proposed. The first suggested limited lateral diatomaceous transport of Navicula species between the Galápagos and continental South America. Alternatively, these new species may be ecological specialists arising from the unique environmental conditions of the Galápagos coastal lagoons, which restrict the colonization of common diatom taxa and enable the establishment of novel, rare species. The Diablas wetlands are an important site for diatom research, where local‐scale environmental changes have combined with global‐scale biogeographic processes resulting in unique diatom assemblages.     

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.     

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.     

<Emphasis Type="Italic">Anthidium vigintiduopunctatum</Emphasis> Friese (Hymenoptera: Megachilidae): the elusive “dwarf bee” of the Galápagos Archipelago?

The endemic large carpenter bee, Xylocopa darwini Cockerell, was the only known pollinator to the Galápagos Archipelago but as early as 1964 locals also spoke of the “dwarf bee of Floreana”. We report the presence of the wool carder bee, Anthidium vigintiduopunctatum Friese, on the island of Floreana and use a species distribution model to predict its distribution in the archipelago. We found that this species has the potential to invade almost one-third the surface area of the Galápagos Archipelago, primarily in low arid areas. Given that wool carder bees are uncommonly collected, we discuss whether this species is a previously undetected native bee or a recent adventive species to the Galápagos.     

Introduction history and genetic diversity of the invasive ant <Emphasis Type="Italic">Solenopsis geminata</Emphasis> in the Galápagos Islands

The Galápagos Islands constitute one of the most pristine tropical systems on Earth. However, the complex and fragile equilibrium of native species is threatened by invasive species, among which is one of the most successful ants in the world, the tropical fire ant, Solenopsis geminata. We characterized the genetic structure and diversity of populations of S. geminata in the Galápagos Islands and unravelled the archipelago colonization by combining Bayesian clustering methods and coalescent-based scenario testing. Using 12 microsatellite markers and one mitochondrial DNA fragment (COI), we analysed individuals collected in all main invaded islands of the archipelago and from the native areas in Costa Rica and mainland Ecuador. We also used mitochondrial DNA to infer evolutionary relationships of samples collected in Galápagos Islands, Ecuador, Costa Rica and other Latin American countries. Our results showed that genetic diversity was significantly lower in Galápagos Islands and mainland Ecuador populations when compared to Costa Rican populations, and that samples from Galápagos Islands and mainland Ecuador (Guayaquil) clustered in a single group and all share a single mtDNA haplotype. Approximate Bayesian Computation favoured a scenario assuming that populations from Galápagos Islands diverged from mainland Ecuador. The city of Guyaquil, an obligatory hub for tourism and trade, could act as a bridgehead.     

Genetic distinctiveness of brown pelicans (<Emphasis Type="Italic">Pelecanus occidentalis</Emphasis>) from the Galápagos Islands compared to continental North America

We examined population differentiation across a substantial portion of the range of the brown pelican (Pelecanus occidentalis) to assess (1) the genetic distinctness of the Galápagos subspecies (P. o. urinator) and (2) genetic differentiation between subspecies that inhabit the coasts of North and Central America (P. o. californicus and P. o. carolinensis). Birds were sampled from coastal California, coastal Florida, and the Galápagos Islands. Using a 957 bp (bp) fragment of the NADH dehydrogenase subunit 2 (ND2) gene, 661 bp of the mitochondrial control region, and eleven microsatellite loci we characterize population genetic differentiation among 158 brown pelicans. The Galápagos subspecies is genetically distinct from the sampled continental subspecies, possessing a unique ND2 haplotype and unique mitochondrial control region haplotypes. Samples from the two continental subspecies all possessed the same ND2 haplotype and shared four mitochondrial control region haplotypes. Bayesian clustering in STRUCTURE placed the Galápagos subspecies in a distinct genetic group with high probability, but could not differentiate the continental subspecies from one another. Estimates of migration rates from BayesAss indicated substantial migration between continental subspecies, but no migration between the Galápagos subspecies and either continental subspecies. There are clearly two Evolutionarily Significant Units within the range of the brown pelican, which warrants conservation attention. Further investigation should determine how the un-sampled subspecies (P. o. murphyi and P. o. occidentalis) fit into the broader picture.     

Characterization of canarypox-like viruses infecting endemic birds in the Galápagos Islands

The presence of avian pox in endemic birds in the Galápagos Islands has led to concern that the health of these birds may be threatened by avipoxvirus introduction by domestic birds. We describe here a simple polymerase chain reaction-based method for identification and discrimination of avipoxvirus strains similar to the fowlpox or canarypox viruses. This method, in conjunction with DNA sequencing of two polymerase chain reaction-amplified loci totaling about 800 bp, was used to identify two avipoxvirus strains, Gal1 and Gal2, in pox lesions from yellow warblers (Dendroica petechia), finches (Geospiza spp.), and Galápagos mockingbirds (Nesomimus parvulus) from the inhabited islands of Santa Cruz and Isabela. Both strains were found in all three passerine taxa, and sequences from both strains were less than 5% different from each other and from canarypox virus. In contrast, chickens in Galápagos were infected with a virus that appears to be identical in sequence to the characterized fowlpox virus and about 30% different from the canarypox/Galápagos group viruses in the regions sequenced. These results indicate the presence of canarypox-like viruses in endemic passerine birds that are distinct from the fowlpox virus infecting chickens on Galápagos. Alignment of the sequence of a 5.9-kb region of the genome revealed that sequence identities among Gal1, Gal2, and canarypox viruses were clustered in discrete regions. This indicates that recombination between poxvirus strains in combination with mutation led to the canarypox-like viruses that are now prevalent in the Galápagos.     

Heterospecific alarm call recognition in a non-vocal reptile

The ability to recognize and respond to the alarm calls of heterospecifics has previously been described only in species with vocal communication. Here we provide evidence that a non-vocal reptile, the Galápagos marine iguana (Amblyrhynchus cristatus), can eavesdrop on the alarm call of the Galápagos mockingbird (Nesomimus parvulus) and respond with anti-predator behaviour. Eavesdropping on complex heterospecific communications demonstrates a remarkable degree of auditory discrimination in a non-vocal species.     

Tracing early stages of species differentiation: Ecological,morphological and genetic divergence of Galápagos sea lion populations

Background  

Oceans are high gene flow environments that are traditionally believed to hamper the build-up of genetic divergence. Despite this, divergence appears to occur occasionally at surprisingly small scales. The Galápagos archipelago provides an ideal opportunity to examine the evolutionary processes of local divergence in an isolated marine environment. Galápagos sea lions (Zalophus wollebaeki) are top predators in this unique setting and have an essentially unlimited dispersal capacity across the entire species range. In theory, this should oppose any genetic differentiation.