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.     

Darwin's Galápagos finches in modern biology

One of the classic examples of adaptive radiation under natural selection is the evolution of 15 closely related species of Darwin''s finches (Passeriformes), whose primary diversity lies in the size and shape of their beaks. Since Charles Darwin and other members of the Beagle expedition collected these birds on the Galápagos Islands in 1835 and introduced them to science, they have been the subjects of intense research. Many biology textbooks use Darwin''s finches to illustrate a variety of topics of evolutionary theory, such as speciation, natural selection and niche partitioning. Today, as this Theme Issue illustrates, Darwin''s finches continue to be a very valuable source of biological discovery. Certain advantages of studying this group allow further breakthroughs in our understanding of changes in recent island biodiversity, mechanisms of speciation and hybridization, evolution of cognitive behaviours, principles of beak/jaw biomechanics as well as the underlying developmental genetic mechanisms in generating morphological diversity. Our objective was to bring together some of the key workers in the field of ecology and evolutionary biology who study Darwin''s finches or whose studies were inspired by research on Darwin''s finches. Insights provided by papers collected in this Theme Issue will be of interest to a wide audience.     

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.     

Ecosystem resilience and threshold response in the Galápagos coastal zone

Background

The Intergovernmental Panel on Climate Change (IPCC) provides a conservative estimate on rates of sea-level rise of 3.8 mm yr⁻¹ at the end of the 21^st century, which may have a detrimental effect on ecologically important mangrove ecosystems. Understanding factors influencing the long-term resilience of these communities is critical but poorly understood. We investigate ecological resilience in a coastal mangrove community from the Galápagos Islands over the last 2700 years using three research questions: What are the ‘fast and slow’ processes operating in the coastal zone? Is there evidence for a threshold response? How can the past inform us about the resilience of the modern system?

Methodology/Principal Findings

Palaeoecological methods (AMS radiocarbon dating, stable carbon isotopes (δ¹³C)) were used to reconstruct sedimentation rates and ecological change over the past 2,700 years at Diablas lagoon, Isabela, Galápagos. Bulk geochemical analysis was also used to determine local environmental changes, and salinity was reconstructed using a diatom transfer function. Changes in relative sea level (RSL) were estimated using a glacio-isostatic adjustment model. Non-linear behaviour was observed in the Diablas mangrove ecosystem as it responded to increased salinities following exposure to tidal inundations. A negative feedback was observed which enabled the mangrove canopy to accrete vertically, but disturbances may have opened up the canopy and contributed to an erosion of resilience over time. A combination of drier climatic conditions and a slight fall in RSL then resulted in a threshold response, from a mangrove community to a microbial mat.

Conclusions/Significance

Palaeoecological records can provide important information on the nature of non-linear behaviour by identifying thresholds within ecological systems, and in outlining responses to ‘fast’ and ‘slow’ environmental change between alternative stable states. This study highlights the need to incorporate a long-term ecological perspective when designing strategies for maximizing coastal resilience.     

Understanding the colonization history of the Galápagos flycatcher (Myiarchus magnirostris)

The Galápagos archipelago has never been connected to any continental land masses, so it is of interest to know the colonization and diversification history of its endemic species. We analyzed the phylogenetic placement of the endemic Galápagos flycatcher, M. magnirostris, within Myiarchus by using the genes ND2 and cytb (1970 bp) to compare 16 of the 22 species that comprise this genus. We also analyzed variability in cytb sequences from 154 M. magnirostris individuals captured on seven Galápagos islands. Our phylogenetic analyses recovered the two main Myiarchus clades that had been described by previous genetic, morphological, and vocal analyses. M. magnirostris is monophyletic and its closest living relative is M. tyrannulus from Mexico and Central America. The average age for the split node between these two groups was approximately 850,000 years (95% C.I. 630,735-1,087,557). M. tyrannulus, M. nugator, M. nuttingi, M. sagrae, and M. stolidus are not monophyletic species. Within M. magnirostris itself, we found low nucleotide and haplotype diversities (π=0.0009 and h=0.4913, respectively) and a high genetic structure among populations. We also detected a star-shaped haplotype network and significantly negative values for Tajima's D and Fu's Fs for this species. Our results suggest that M. magnirostris originated from a single colonization event and had a recent population expansion in the Galápagos archipelago.     

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.     

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.     

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.

     

Ecosystem changes in Galápagos highlands by the invasive tree Cinchona pubescens

Background and aims

Salinity is an increasing problem for agricultural production worldwide. Understanding how Na⁺ enters plants is important if reducing Na⁺ influx, a key component of the regulation of Na⁺ accumulation in plants and improving salt tolerance of crop plants, is to be achieved. Our previous work indicated that two distinct low-affinity Na⁺ uptake pathways exist in the halophyte Suaeda maritima. Here, we report the external NaCl concentration at which uptake switches from pathway 1 to pathway 2 and the kinetics of the interaction between external K⁺ concentration and Na⁺ uptake and accumulation in S. maritima in order to determine the roles of K⁺ transporters or channels in low-affinity Na⁺ uptake.

Methods

Na⁺ influx, Na⁺ and K⁺ accumulations in S. maritima exposed to various concentrations of NaCl (0–200 mM) were analyzed in the absence and presence of the inhibitors TEA and Ba⁺ (5 mM TEA or 3 mM Ba²⁺) or KCl (0, 10 or 50 mM).

Results

Our earlier proposal was confirmed and extended that there are two distinct low-affinity Na⁺ uptake pathways in S. maritima: pathway 1 might be mediated by a HKT-type transporter under low salinity conditions and pathway 2 by an AKT1-type channel or a KUP/HAK/KT type transporter under high salinity conditions. The external NaCl concentration at which two distinct low-affinity Na⁺ uptake switches from pathway 1 to pathway 2, the ‘turning point’, is between 90 and 95 mM. Over a short period (12 h) of Na⁺ and K⁺ treatments, a low concentration of K⁺ (10 mM) facilitated Na⁺ uptake by S. maritima under high salinity (100–200 mM NaCl), whether or not the plants had been subjected to a longer (3 d) period of K⁺ starvation. The kinetics suggests that low concentration of K⁺ (10 mM) might activate AKT1-type channels or KUP/HAK/KT-type transporters under high salinity (100–200 mM NaCl).

Conclusions

The turning-point of external NaCl concentrations for the two low-affinity Na⁺ uptake pathways in Suaeda maritima is between 90 and 95 mM. A low concentration of K⁺ (10 mM) might activate AKT1 or KUP/HAK/KT and facilitate Na⁺ uptake under high salinity (100–200 mM NaCl). The kinetics of K⁺ on Na⁺ uptake and accumulation in S maritima are also consistent with there being two low-affinity Na⁺ uptake pathways.     

Digesta retention time in the Galápagos tortoise (Chelonoidis nigra)

The retention time of food in the digestive tract of animals has important implications for digestive physiology. Retention time impacts digestive efficiency and among herbivores affects plant–animal interactions including herbivory and seed dispersal. Poorly studied yet iconic Galápagos tortoises are large-bodied generalist herbivores and ecosystem engineers which migrate seasonally. Potentially variable digesta retention times due to strong seasonal and altitudinal temperature gradients may influence tortoise seed dispersal abilities and rates of herbivory. We fed captive adult tortoises living in semi-natural conditions on Galápagos with inert particles and seeds from locally available fruits to determine whether seed size and ambient temperature influenced retention time. Median retention time varied from 6 to 28 days, with a mode of 12 days. Seed size had no effect on any of our measures of retention time, but ambient temperature was inversely correlated with retention times. Long retention time facilitates long distance seed dispersal by Galápagos tortoises, which may improve effectiveness. The effect of temperature, which may double from hot lowlands to cold highlands through the seasonal cycle, on tortoise digesta retention time will strongly influence seed dispersal efficiency and may influence patterns of food selection and migration in this species.     

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.     

Effects of the lunar cycle on the Galápagos fur seal,Arctocephalus galapagoensis

Summary During the 1977 and 1979 reproductive periods of the Galápagos fur seals a census taken in the mornings and evenings at Cabo Hammond, Fernandina, showed a marked, synodic lunar rhythm in numbers of animals ashore. About twice as many fur seals were ashore at full moon than at new moon. By use of two independent Fourier analysis methods, the curve of the morning counts is shown to lag 15°–20° of the lunar month behind the curve of the evening counts. The lunar effect is demonstrated for males, females, and immatures. The rhythm is also seen is demonstrated for males, females, and immatures. The rhythm is also seen in attendance data from 13 individually marked females, all but one nursing young. Reproductive events show the lunar rhythm much less markedly than do numbers ashore. This and the clear rhythm in immature numbers make it very likely that the rhythm is a year-round phenomenon, independent of reproduction.There is no reason to assume that fur seals stay on land during moonlit nights especially for social interaction. It is then hypothesized that fur seals avoid moonlight at sea. If so, the peak of numbers ashore at full moon and the negative phase angle difference of the evening curve against the morning curve can be explained with the shift, and the varying duration and brightness, of the moonlit part of the night over the lunar cycle. Two hypotheses which might account for this moonlight avoidance are discussed: (1) predator (shark) avoidance and (2) varying feeding efficiency of the fur seals due to the influence of moonlight on the vertical distribution of prey.     

A comparison of genetic diversity between the Galápagos Penguin and the Magellanic Penguin

The Galápagos Penguin (Spheniscusmendiculus) is a United States federallylisted endangered species with populations onthe Galápagos Islands of Fernandina andIsabela. Although the waters around theislands are normally productive, lowproductivity during El Niño years resultsin high adult penguin mortality and lowrecruitment in following years. We usedmicrosatellite markers developed for Spheniscus penguins to study the long termgenetic effects of serial bottleneck events inthe Galápagos Penguin, and compared thisvariation to that of its congener, theMagellanic penguin (Spheniscusmagellanicus). The observed heterozygosityfor the Galápagos Penguin was 3%,significantly lower than the 46%heterozygosity of the Magellanic Penguin. Thislow level of heterozygosity is directly relatedto its low effective population size. Whilethis population has survived long term,presumably without high levels of geneticvariation, we feel that the greater frequencyof El Niño events, coupled with increasedhuman impacts such as introduced disease, oildischarge, and competition with fisheries, mayput the species in particular danger ofextinction.     

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.     

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.     

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.