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.     

Hematology, serum chemistry, and serology of Galápagos penguins (Spheniscus mendiculus) in the Galápagos Islands, Ecuador

The Galápagos penguin (Spheniscus mendiculus) is an endangered species endemic to the Galápagos Islands, Ecuador. In 2003 and 2004, 195 penguins from 13 colonies on the islands of Isabela and Fernandina in the Galápagos archipelago were examined. Genetic sexing of 157 penguins revealed 62 females and 95 males. Hematology consisted of packed cell volume (n = 134), white blood cell differentials (n = 83), and hemoparasite blood smear evaluation (n = 114). Microfilariae were detected in 22% (25/114) of the blood smears. Female penguins had significantly higher eosinophil counts than males. Serum chemistry on 83 penguins revealed no significant differences between males and females. Birds were seronegative to avian paramyxovirus type 1-3, avian influenza virus, infectious bursal disease virus, Marek's disease virus (herpes), reovirus, avian encephalomyelitis virus, and avian adenovirus type 1 and 2 (n = 75), as well as to West Nile virus (n = 87), and Venezuelan, western and eastern equine encephalitis viruses (n = 26). Seventy-five of 84 (89%) penguins had antibodies to Chlamydophila psittaci but chlamydial DNA was not detected via polymerase chain reaction in samples from 30 birds.     

Hormonal correlates of siblicide in Galápagos Nazca boobies

Nazca boobies (Sula granti) show unconditional obligate siblicide immediately after hatching, reducing the typical two-egg clutch size to one. We studied body mass changes and levels of testosterone (T), corticosterone (CORT), and progesterone (P) for A-chicks (dominant, first hatched), B-chicks (subordinate, second hatched), and singletons, during the first 7 days after hatching, when siblicide normally occurs. Mass increase with age was higher for A-chicks than for singletons and B-chicks. This exaggerated the existing developmental advantage of A- over B-chicks that is due to hatching asynchrony. In nests with two chicks, CORT titer was significantly higher in B-chicks than in A-chicks. During ontogenetic development, CORT decreased with age for A-chicks, but did not change for singletons. P showed qualitatively similar ontogenetic changes to CORT, remaining unchanged for A-chicks but increasing for singletons. Thus, both CORT and P levels were lower for A-chicks than for singletons, and both hormones varied inversely with body mass. Overall, T levels did not differ between different categories of chicks. However, one B-chick in the process of reversing the dominance relationship with its older, but weakened, sibling had significantly elevated T. We suggest that CORT and P are regulated to promote exaggerated mass gain in socially challenged A-chicks, facilitating siblicide. Whether T induces aggressiveness during short time intervals of intense sibling rivalry needs further attention.     

A cryptic taxon of Galápagos tortoise in conservation peril

As once boldly stated, 'bad taxonomy can kill', highlighting the critical importance of accurate taxonomy for the conservation of endangered taxa. The concept continues to evolve almost 15 years later largely because most legal protections aimed at preserving biological diversity are based on formal taxonomic designations. In this paper we report unrecognized genetic divisions within the giant tortoises of the Galápagos. We found three distinct lineages among populations formerly considered a single taxon on the most populous and accessible island of Santa Cruz; their diagnosability, degree of genetic divergence and phylogenetic placement merit the recognition of at least one new taxon. These results demonstrate the fundamental importance of continuing taxonomic investigations to recognize biological diversity and designate units of conservation, even within long-studied organisms such as Galápagos tortoises, whose evolutionary heritage and contribution to human intellectual history warrant them special attention.     

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.     

Teaching the tourists in Galápagos: what do Galápagos National Park guides know,think, and teach tourists about evolution?

Background

Evolution is everywhere in Galápagos, especially regarding the role the islands have played in the history of evolutionary thought. In turn, the Galápagos National Park guides are in a unique position as informal science educators, as they are the primary points-of-contact for the islands’ ~ 200,000 tourists per year. Our goal was to assess the guides’ knowledge and acceptance of the theory of evolution, in addition to learning more about their perceptions of the connection between the islands and evolution.

Methods

We surveyed 63 guides in three towns on three of the archipelago’s populated islands. Surveys included items targeting the guides knowledge of evolution (via the Knowledge of Evolution Exam, or the KEE) and acceptance of the theory of evolution (via the Measure of Acceptance of the Theory of Evolution, or the MATE). Additional, novel items gauged the guides’ perceptions of the islands, insofar as Galápagos is connected to evolution and the history of evolutionary thought.

Results

Although acceptance of evolution was high, knowledge was relatively low. However, the guides are proud of the islands’ association with the history of evolutionary thought, and enjoy talking about evolution while giving tours. On open-ended responses, guides claimed to especially enjoy talking with tourists about geology and island culture, and a few voiced concerns about the conflict between evolution and religion. Finally, the overwhelming majority of the guides agreed or strongly agreed with the statement, “I would like to learn more about Galápagos and the history of evolutionary thought.”

Conclusions

Galápagos guides display a disconnect between what is felt about evolution, and what is known about how evolution actually works. We can probably trace their fondness for, and acceptance of, evolution to the clear connection between evolution, tourism, and the guides’ livelihoods. We can trace their lack of knowledge to their schooling, as prior work detected similarly low knowledge of evolution in the islands’ schoolteachers. However, the guides are a receptive audience for professional development pertaining to our contemporary understanding of the mechanics of biological evolution. Improving guides’ understanding of biological evolution could, in turn, inform the evolutionary understanding of thousands of tourists each year.

     

Ancient DNA gives green light to Galápagos Land Iguana repatriation

Land Iguanas, Conolophus subcristatus,were extirpated from Isla Baltra, GalápagosArchipelago in the 1940s. Historical recordsindicate that some Baltra iguanas weretranslocated to nearby Isla Seymour Norte inthe 1930s. Plans to repatriate iguanas toBaltra were suspended when evidence suggestedthat iguanas on Seymour Norte may not beentirely of Baltra origin. Comparison of DNAfrom century-old museum specimens with extantiguanas has identified those individuals ofunambiguous Baltra origin on Seymour Norte. These results provide scientific criteria forthe ecological restoration of these endangeredreptiles.     

Phylogeography and history of giant Galápagos tortoises

Abstract.— We examined the phylogeography and history of giant Galàpagos tortoise populations based on mito-chondrial DNA sequence data from 161 individuals from 21 sampling sites representing the 11 currently recognized extant taxa. Molecular clock and geological considerations indicate a founding of the monophyletic Galàpagos lineage around 2–3 million years ago, which would allow for all the diversification to have occurred on extant islands. Founding events generally occurred from geologically older to younger islands with some islands colonized more than once. Six of the 11 named taxa can be associated with monophyletic maternal lineages. One, Geochelone porteri on Santa Cruz Island, consists of two distinct populations connected by the deepest node in the archipelago-wide phylogeny, whereas tortoises in northwest Santa Cruz are closely related to those on adjacent Pinzón Island. Volcan Wolf, the northernmost volcano of Isabela Island, consists of both a unique set of maternal lineages and recent migrants from other islands, indicating multiple colonizations possibly due to human transport or multiple colonization and partial elimination through competition. These genetic findings are consistent with the mixed morphology of tortoises on this volcano. No clear genetic differentiation between two taxa on the two southernmost volcanoes of Isabela was evident. Extinction of crucial populations by human activities confounds whether domed versus saddleback carapaces of different populations are mono- or polyphyletic. Our findings revealed a complex phylogeography and history for this tortoise radiation within an insular environment and have implications for efforts to conserve these endangered biological treasures.     

Historic fuel wood use in the Galápagos Islands: identification of charred remains

Charcoal fragments from five historic campsite locations in the Galápagos Islands were identified and radiocarbon dated to investigate postulated early human presence in the archipelago, historic fuel wood collection patterns and the resultant impact on native vegetation. A variety of taxa and fuel types were revealed to be present in the charcoal assemblages, indicating geographically driven rather than species-specific methods of collection. Historic anthropogenic impact was therefore spread amongst woody taxa in the lowland plant communities, with severity dependent on proximity to campsite location. All charred remains were found to date from within the historic period, supporting the preponderance of archaeological evidence indicating that human presence did not begin in Galápagos until after European discovery.     

Experimental studies of rapid bioerosion of coral reefs in the Galápagos Islands

Experimental carbonate blocks of coral skeleton,Porites lobata (PL), and cathedral limestone (LS) were deployed for 14.8 months at shallow (5–6 m) and deep (11–13m) depths on a severely bioeroded coral reef, Champion Island, Galápagos Islands, Ecuador. Sea urchins (Eucidaris thouarsii) were significantly more abundant at shallow versus deep sites.Porites lobata blocks lost an average of 25.4 kg m^–2yr^–1 (23.71 m^–2yr^–1 or 60.5% decrease yr^–1). Losses did not vary significantly at depths tested. Internal bioeroders excavated an average of 2.6 kg m^–2 yr^–1 (2.41 m^–2 yr^–1 or 0.6% decrease yr^–1), while external bioeroders removed an average of 22.8 kg m^–2 yr^–1). (21.31 m^–2 yr^–1). or 59.9% decrease yr^–1). few encrusting organisms were observed on the PL blocks. Cathedral limestone blocks lost an average of 4.1 kg m^–2 yr^–1). (1.81 m^–2 yr^–1). or 4.6% decrease yr-'), also with no relation to depth. Internal bioeroders excavated an average of 0.6 kg m^–2 yr^–1). (0.31 m^–2 yr^–1). or 0.7% decrease yr^–1). and external bioeroders removed an average of 3.5 kg m^–2 yr^–1). (1.51 m^–2 yr^–1). or 3.9% decrease yr^–1). from the LS blocks. Most (57.6%) encrustation occurred on the bottom of LS blocks, and there was more accretion on block bottoms in deep (61.4 mg cm^–2 yr^–1). versus shallow (35.0 mg cm^–2 yr^–1) sites. External bioerosion reduced the average height of the reef framework by 0.2 cm yr^–1). for hard substrata (represented by LS) and 2.3 cm yr^–1). for soft substrata (represented by PL). The results of this study suggest that coral reef frameworks in the Galápagos Islands are in serious jeopardy. If rates of coral recruitment do not increase, and if rates of bioerosion do not decline, coral reefs in the Galápagos Islands could be eliminated entirely.     

The Galápagos Islands: biogeographic patterns and geology

In the traditional biogeographic model, the Galápagos Islands appeared a few million years ago in a sea where no other islands existed and were colonized from areas outside the region. However, recent work has shown that the Galápagos hotspot is 139 million years old (Early Cretaceous), and so groups are likely to have survived at the hotspot by dispersal of populations onto new islands from older ones. This process of metapopulation dynamics means that species can persist indefinitely in an oceanic region, as long as new islands are being produced. Metapopulations can also undergo vicariance into two metapopulations, for example at active island arcs that are rifted by transform faults. We reviewed the geographic relationships of Galápagos groups and found 10 biogeographic patterns that are shared by at least two groups. Each of the patterns coincides spatially with a major tectonic structure; these structures include: the East Pacific Rise; west Pacific and American subduction zones; large igneous plateaus in the Pacific; Alisitos terrane (Baja California), Guerrero terrane (western Mexico); rifting of North and South America; formation of the Caribbean Plateau by the Galápagos hotspot, and its eastward movement; accretion of Galápagos hotspot tracks; Andean uplift; and displacement on the Romeral fault system. All these geological features were active in the Cretaceous, suggesting that geological change at that time caused vicariance in widespread ancestors. The present distributions are explicable if ancestors survived as metapopulations occupying both the Galápagos hotspot and other regions before differentiating, more or less in situ.     

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.     

Genetic analysis of a successful repatriation programme: giant Galápagos tortoises

As natural populations of endangered species dwindle to precarious levels, remaining members are sometimes brought into captivity, allowed to breed and their offspring returned to the natural habitat. One goal of such repatriation programmes is to retain as much of the genetic variation of the species as possible. A taxon of giant Galápagos tortoises on the island of Espa?ola has been the subject of a captive breeding-repatriation programme for 33 years. Core breeders, consisting of 12 females and three males, have produced more than 1200 offspring that have been released on Espa?ola where in situ reproduction has recently been observed. Using microsatellite DNA markers, we have determined the maternity and paternity of 132 repatriated offspring. Contributions of the breeders are highly skewed. This has led to a further loss of genetic variation that is detrimental to the long-term survival of the population. Modifications to the breeding programme could alleviate this problem.     

Colonization history, ecological shifts and diversification in the evolution of endemic Galápagos weevils

Mitochondrial DNA sequence data were obtained for eight species of flightless Galapaganus endemic weevils and one winged close relative in order to study their colonization history and modes of diversification in the Galápagos Archipelago. Contrary to most other insular radiations, the phylogeny estimates we recovered for Galapaganus do not follow the progression rule of island biogeography. The penalized likelihood age estimates of colonization of the archipelago exceed the age of the emerged islands and underscore the potential role of now sunken seamounts for the early evolution of Galapaganus . The phylogeny proposes one intra-island origin for Galapaganus endemics, but monophyly tests suggest a larger contribution of in-situ speciation on older islands. Generalist habitat preferences were reconstructed as ancestral while shifts to highland habitats were reconstructed as having evolved independently on different islands. Magnitudes and patterns of diversification rate were found to differ between older and younger islands. Our analyses reveal that the colonization sequence of islands and timing of colonization of Galapaganus could be linked with the geological and volcanic history of the islands in a rather complex scenario. Even though most islands appear to have been colonized soon after their emergence, there are notable deviations from the pattern of sequential colonization expected under the progression rule when considering only the extant emerged islands. Patterns of diversification rate variation on older and younger islands correspond to the volcanic activity or remnants of such activity, while the pattern of independent evolution of restricted habitat preferences in different islands suggests that habitat shifts could also have contributed to species diversity in Galapaganus .     

Current status of alien vertebrates in the Galápagos Islands: invasion history, distribution, and potential impacts

Human activity has promoted the invasion of the Galápagos Islands by alien species from each of the five classes of vertebrates. We review the current distribution of alien vertebrates in the archipelago, their impacts on native species, and management efforts aimed at alien vertebrates. A total of 44 species have been reported in the archipelago, with 20 species establishing feral populations. Mammals were the first group arriving in the archipelago and remain the most numerous, with 10 established species. Alien birds invaded after mammals and four species have established populations. Reptiles, amphibians, and fish invaded later and are represented by three, one, and two species, respectively. Alien mammals are the most injurious to native biota, contributing to the decline or extinction of several species. Aside from mammals, no other class of alien vertebrate has had documented impacts on native species. Several populations of large and medium-sized mammals and birds have been eradicated.     

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.     

Pollination patterns and plant breeding systems in the Galápagos: a review

Background

Despite the importance of the Galápagos Islands for the development of central concepts in ecology and evolution, the understanding of many ecological processes in this archipelago is still very basic. One such process is pollination, which provides an important service to both plants and their pollinators. The rather modest level of knowledge on this subject has so far limited our predictive power on the consequences of the increasing threat of introduced plants and pollinators to this unique archipelago.

Scope

As a first step toward building a unified view of the state of pollination in the Galápagos, a thorough literature search was conducted on the breeding systems of the archipelago''s flora and compiled all documented flower–visitor interactions. Based on 38 studies from the last 100 years, we retrieved 329 unique interactions between 123 flowering plant species (50 endemics, 39 non-endemic natives, 26 introduced and eight of unknown origin) from 41 families and 120 animal species from 13 orders. We discuss the emergent patterns and identify promising research avenues in the field.

Conclusions

Although breeding systems are known for <20 % of the flora, most species in our database were self-compatible. Moreover, the incidence of autogamy among endemics, non-endemic natives and alien species did not differ significantly, being high in all groups, which suggests that a poor pollinator fauna does not represent a constraint to the integration of new plant species into the native communities. Most interactions detected (approx. 90 %) come from a single island (most of them from Santa Cruz). Hymenopterans (mainly the endemic carpenter bee Xylocopa darwinii and ants), followed by lepidopterans, were the most important flower visitors. Dipterans were much more important flower visitors in the humid zone than in the dry zone. Bird and lizard pollination has been occasionally reported in the dry zone. Strong biases were detected in the sampling effort dedicated to different islands, time of day, focal plants and functional groups of visitors. Thus, the existing patterns need to be confronted with new and less biased data. The implementation of a community-level approach could greatly increase our understanding of pollination on the islands and our ability to predict the consequences of plant invasions for the natural ecosystems of the Galápagos.     

Hybridization masks speciation in the evolutionary history of the Galápagos marine iguana

The effects of the direct interaction between hybridization and speciation—two major contrasting evolutionary processes—are poorly understood. We present here the evolutionary history of the Galápagos marine iguana (Amblyrhynchus cristatus) and reveal a case of incipient within-island speciation, which is paralleled by between-island hybridization. In-depth genome-wide analyses suggest that Amblyrhynchus diverged from its sister group, the Galápagos land iguanas, around 4.5 million years ago (Ma), but divergence among extant populations is exceedingly young (less than 50 000 years). Despite Amblyrhynchus appearing as a single long-branch species phylogenetically, we find strong population structure between islands, and one case of incipient speciation of sister lineages within the same island—ostensibly initiated by volcanic events. Hybridization between both lineages is exceedingly rare, yet frequent hybridization with migrants from nearby islands is evident. The contemporary snapshot provided by highly variable markers indicates that speciation events may have occurred throughout the evolutionary history of marine iguanas, though these events are not visible in the deeper phylogenetic trees. We hypothesize that the observed interplay of speciation and hybridization might be a mechanism by which local adaptations, generated by incipient speciation, can be absorbed into a common gene pool, thereby enhancing the evolutionary potential of the species as a whole.