Equilibrium and non‐equilibrium dynamics simultaneously operate in the Galápagos islands

Island biotas emerge from the interplay between colonisation, speciation and extinction and are often the scene of spectacular adaptive radiations. A common assumption is that insular diversity is at a dynamic equilibrium, but for remote islands, such as Hawaii or Galápagos, this idea remains untested. Here, we reconstruct the temporal accumulation of terrestrial bird species of the Galápagos using a novel phylogenetic method that estimates rates of biota assembly for an entire community. We show that species richness on the archipelago is in an ascending phase and does not tend towards equilibrium. The majority of the avifauna diversifies at a slow rate, without detectable ecological limits. However, Darwin's finches form an exception: they rapidly reach a carrying capacity and subsequently follow a coalescent‐like diversification process. Together, these results suggest that avian diversity of remote islands is rising, and challenge the mutual exclusivity of the non‐equilibrium and equilibrium ecological paradigms.     

Seasonal reproductive cycle of the Galápagos tortoise (Geochelone nigra) in captivity

The reproductive physiology of nine Galápagos tortoises (Geochelone nigra) was studied from February 1988 to May 1989. The study encompassed the annual reproductive cycle to include complete mating and nesting sequences. Male (n = 4) and female (n = 5) seasonal reproductive changes were determined throughout the study with endocrine analysis and ultrasonographic examinations. Males displayed a prenuptial rise in serum testosterone (x― ±SE = 6.62 ± 0.92 ng/ml in August) during which gonadal maturation and spermatogenesis are thought to occur. The male reproductive cycle appears consistent with the prenuptial spermatogenic pattern exhibited by other tropical turtles. In the females, testosterone rose during the mating period (x― ± SE = 499.3 ± 124.6 pg/ml in October) prior to ovulation and is probably related to receptivity in the females. Progesterone was more variable, but also peaked during the mating period (x― ± SE = 1,017.2 ± 220.6 pg/ml in October) and appears related to ovulation. Estradiol rose several months prior to mating (x― ± SE = 75.5 ± 11.9 pg/ml in July) and was correlated with increased serum calcium levels. This increase in estradiol is thought to stimulate vitellogenesis several months prior to mating. Nesting occurred from November 1988 to April 1989, during which six clutches were laid. Clutch size ranged from eight to 17 eggs. Both male and female Galápagos tortoises display seasonal physiological changes that function to regulate annual reproductive patterns. Zoo Biol 17:505–517, 1998. © 1998 Wiley-Liss, Inc.     

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.     

Persistent inter‐ and intraspecific gene exchange within a parallel radiation of caterpillar hunter beetles (Calosoma sp.) from the Galápagos

When environmental gradients are repeated on different islands within an archipelago, similar selection pressures may act within each island, resulting in the repeated occurrence of ecologically similar species on each island. The evolution of ecotypes within such radiations may either result from dispersal, that is each ecotype evolved once and dispersed to different islands where it colonized its habitat, or through repeated and parallel speciation within each island. However, it remains poorly understood how gene flow during the divergence process may shape such patterns. In the Galápagos islands, three phenotypically similar species of the beetle genus Calosoma occur at higher elevations of different islands, while lowlands are occupied by a fourth species. By genotyping all major populations within this radiation for two nuclear and three mitochondrial gene fragments and seven microsatellite markers, we found strong support that the oldest divergence separates the highland species of the oldest island from the remaining species. Despite their morphological distinctness, highland species of the remaining islands were genetically closely related to the lowland population on each island and within the same magnitude as lowland populations sampled at different islands. Repeated evolution of highland ecotypes out of the lowland species appears the most likely scenario and estimates of geneflow rates revealed extensive admixture among ecotypes within islands, as well as between islands. These findings indicate that gene exchange among the different populations and species may have shaped the phylogenetic relationships and the repeated evolution of these ecotypes.     

The phylogenetic position of the Galápagos Cormorant

The endangered Galápagos Cormorant, Phalacrocorax harrisi, is unique among the species of the Phalacrocoracidae in being flightless and sequentially polyandrous. It has had a vexed taxonomic history, variously being lumped with all the species in Phalacrocorax, being accorded its own genus, Nannopterum, or being included in Leucocarbo or Compsohalieus. Different authorities have similarly suggested a number of different species as being its closest relative. Here we use novel mitochondrial DNA sequence data to show that the Galápagos Cormorant is related to the sister pair of the mainland Americas, the Double-crested Cormorant, P. auritus, and the Neotropic Cormorant, P. brasilianus. This trio of species has high statistical support (Bayesian posterior probability of 1.00; NJ bootstrap 98%; MP bootstrap 91%). The Galápagos Cormorant is thus a relatively recent offshoot of the mainland form, which has subsequently evolved flightlessness. Until the phylogeny of the cormorants is more clearly resolved, we recommend the continued use of Phalacrocorax for all species.     

Parallel habitat specialization within the wolf spider genus Hogna from the Galápagos

Within most island archipelagos, such as the Galápagos, similar ecological gradients are found on geographically isolated islands. Species radiations in response to these ecological gradients may follow different scenarios being (i) a single habitat specialization event followed by secondary colonization of each ecotype on the different islands or (ii) repeated and parallel habitat specialization on each island separately. This latter scenario has been considered less likely as gene flow might hamper such ecotypic differentiation. At least for the Galápagos, the extent to which this process is involved in species radiations remains yet poorly understood. Within the wolf spider genus Hogna, seven species are described that can be divided into three different ecotypes based on general morphology and habitat preference i.e. species that inhabit the pampa vegetation in the highlands, species that occur in coastal dry habitats and one generalist species. Comparison of the species phylogeny based on one mitochondrial (COI) and one nuclear (28S) gene fragment convincingly demonstrates that ‘pampa’ and ‘coastal dry’ species evolved in parallel on the islands Santa Cruz and San Cristóbal. Despite the observation that allozymes analysis indicated that each species forms a distinct genetic cluster, phylogenetic divergence within these species complexes was very low and paraphyletic and most likely due to hybridization rather than incomplete lineage sorting, as demonstrated for the Santa Cruz species complex. This suggests that within‐island speciation occurred under low levels of gene flow. Species phylogeny in general did not follow the progression of island emergence as a molecular clock analysis suggested that island endemic species may have diverged after as well as before the emergence of the islands. This represents the first clear example of parallel and within‐island speciation because of habitat specialization on the Galápagos and that such divergence most likely occurred under historic gene flow.     

Evolution on oceanic islands: molecular phylogenetic approaches to understanding pattern and process

By their very nature oceanic island ecosystems offer great opportunities for the study of evolution and have for a long time been recognized as natural laboratories for studying evolution owing to their discrete geographical nature and diversity of species and habitats. The development of molecular genetic methods for phylogenetic reconstruction has been a significant advance for evolutionary biologists, providing a tool for answering questions about the diversity among the flora and fauna on such islands. These questions relate to both the origin and causes of species diversity both within an archipelago and on individual islands. Within a phylogenetic framework one can answer fundamental questions such as whether ecologically and/or morphologically similar species on different islands are the result of island colonization or convergent evolution. Testing hypotheses about ages of the individual species groups or entire community assemblages is also possible within a phylogenetic framework. Evolutionary biologists and ecologists are increasingly turning to molecular phylogenetics for studying oceanic island plant and animal communities and it is important to review what has been attempted and achieved so far, with some cautionary notes about interpreting phylogeographical pattern on oceanic islands.     

Darwin's finches: a model of landscape effects on metacommunity dynamics in the Galápagos Archipelago

Darwin's finches represent a dynamic radiation of birds within the Galápagos Archipelago. Unlike classic island radiations dominated by island endemics and intuitive ‘conveyer belt’ colonization with little subsequent dispersal, species of Darwin's finches have populations distributed across many islands and each island contains complex metacommunities of closely related birds. Understanding the role of metacommunity and structured population dynamics in speciation within this heterogeneous island system would provide insights into the roles of fragmentation and dispersal in evolution. In this study, a large multi‐species dataset and a comparative ground finch dataset (two co‐distributed lineages) were used to show how landscape features influence patterns of gene flow across the archipelago. Factors expected to regulate migration including distance and movement from large, central islands to small, peripheral islands were rejected in the multi‐species dataset. Instead, the harsh northeast islands contributed individuals to the larger central islands. Successful immigration relies on three factors: arriving, surviving and reproducing, thus the dispersal towards the central islands may be either be due to more migrants orienting towards these land masses due to their large size and high elevation, or may reflect a higher likelihood of survival and successful reproduction due to the larger diversity of habitats and more environmentally stable ecosystems that these islands possess. Further, the overall directionality of migration was south‐southwest against the dominant winds and currents. In comparing dispersal between the common cactus finch and medium ground finch, both species had similar migration rates but the cactus finch had approximately half the numbers of migrants due to lower effective populations sizes. Significant population structure in the cactus finch indicates potential for further speciation, while the medium ground finch maintains cohesive gene flow across islands. These patterns shed light on the macroevolutionary patterns that drive diversification and speciation within a radiation of highly‐volant taxa.     

The role of spines in anthropogenic seed dispersal on the Galápagos Islands

1. Dispersal has important ecological and evolutionary consequences for populations, but understanding the role of specific traits in dispersal can be difficult and requires careful experimentation. Moreover, understanding how humans alter dispersal is an important question, especially on oceanic islands where anthropogenic disturbance through species introductions can dramatically alter native ecosystems.
2. In this study, we investigated the functional role of spines in seed dispersal of the plant caltrop (Tribulus cistoides L., Zygophyllaceae) by anthropogenic dispersal agents. We also tested whether humans or wildlife are more important seed dispersers of T. cistoides on the Galápagos.
3. Tribulus cistoides is found on tropical mainland and oceanic island habitats. The dispersal structure of T. cistoides is called a mericarp, and they are typically protected by one pair of upper spines and a second pair of lower spines, but the presence and size of spines varies within and between populations. On the Galápagos, the upper and lower spines protect mericarps from seed predation by Darwin's finches. We tested whether spines play a dual role in dispersal by factorially manipulating the presence/absence of the upper and lower spines to simulate natural variation in mericarp morphology.
4. The upper spines greatly facilitated seed dispersal, whereas the lower spines had no discernible effect on dispersal. The presence of upper spines increased dispersal rate on shoes by pedestrians 23‐fold, on fabrics (e.g., towels) and cars by nearly twofold, and the presence of upper spines increased dispersal distance by cars sixfold. When comparing dispersal rates in habitats with high (roads and foot paths) versus low (arid forest) anthropogenic activity, dispersal rates were demonstrably higher in the habitats with more human activity.
5. These results have important implications for understanding the ecology and evolution of plant dispersal in the Anthropocene. Spines on the fruits of T. cistoides play important functional roles in anthropogenic dispersal, whereas native and introduced wildlife plays a minor role in dispersal on inhabited islands of the Galápagos. Our results imply that seed predators and humans are jointly shaping the ecology and evolution of contemporary populations of T. cistoides on the Galápagos.

     

The influence of ecological factors on mosquito abundance and occurrence in Galápagos

We sampled mosquitoes across 18 sites established at different elevations and stretching from the north to the south of Isla Santa Cruz, Galápagos. Two commonly occurring species, Ae. taeniorhynchus and Cx. quinquefasciatus, were collected along with environmental variables characteristic of the trapping sites to assess their influence on mosquito abundance and occurrence in the dry season of 2015. We captured Ae. taeniorhynchus at 14 out of 18 sites and Cx. quinquefasciatus at low and high elevation sites on Santa Cruz. We utilized two generalized linear models; the first assessed the influence of environmental variables on abundances of Ae. taeniorhynchus and the second assessed the influence of these variables on the presence of Cx. quinquefasciatus. Populations of both mosquito species declined with elevation. Rainfall data were limited, as we sampled during the dry season of 2015. Distance to mangroves and maximum humidity were significant in influencing the abundance of Ae. taeniorhynchus, while maximum humidity was found to significantly influence the presence of Cx. quinquefasciatus. Both species occurred in sites where temperature, precipitation, and humidity should allow for mosquito development as well as parasitic development of the protozoan parasites that cause avian malaria. Further research involving year‐round sampling of mosquitoes and accompanying meteorological data as well as experimental studies on vector competence are required to understand disease dynamics of parasites such as avian malaria in Galápagos.     

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.     

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.     

Naturally rare versus newly rare: demographic inferences on two timescales inform conservation of Galápagos giant tortoises

Long‐term population history can influence the genetic effects of recent bottlenecks. Therefore, for threatened or endangered species, an understanding of the past is relevant when formulating conservation strategies. Levels of variation at neutral markers have been useful for estimating local effective population sizes (N_e) and inferring whether population sizes increased or decreased over time. Furthermore, analyses of genotypic, allelic frequency, and phylogenetic information can potentially be used to separate historical from recent demographic changes. For 15 populations of Galápagos giant tortoises (Chelonoidis sp.), we used 12 microsatellite loci and DNA sequences from the mitochondrial control region and a nuclear intron, to reconstruct demographic history on shallow (past ~100 generations, ~2500 years) and deep (pre‐Holocene, >10 thousand years ago) timescales. At the deep timescale, three populations showed strong signals of growth, but with different magnitudes and timing, indicating different underlying causes. Furthermore, estimated historical N_e of populations across the archipelago showed no correlation with island age or size, underscoring the complexity of predicting demographic history a priori. At the shallow timescale, all populations carried some signature of a genetic bottleneck, and for 12 populations, point estimates of contemporary N_e were very small (i.e., < 50). On the basis of the comparison of these genetic estimates with published census size data, N_e generally represented ~0.16 of the census size. However, the variance in this ratio across populations was considerable. Overall, our data suggest that idiosyncratic and geographically localized forces shaped the demographic history of tortoise populations. Furthermore, from a conservation perspective, the separation of demographic events occurring on shallow versus deep timescales permits the identification of naturally rare versus newly rare populations; this distinction should facilitate prioritization of management action.