Hidden variable models reveal the effects of infection from changes in host survival.

The impacts of disease on host vital rates can be demonstrated using longitudinal studies, but these studies can be expensive and logistically challenging. We examined the utility of hidden variable models to infer the individual effects of infectious disease from population-level measurements of survival when longitudinal studies are not possible. Our approach seeks to explain temporal deviations in population-level survival after introducing a disease causative agent when disease prevalence cannot be directly measured by coupling survival and epidemiological models. We tested this approach using an experimental host system (Drosophila melanogaster) with multiple distinct pathogens to validate the ability of the hidden variable model to infer per-capita disease rates. We then applied the approach to a disease outbreak in harbor seals (Phoca vituline) that had data on observed strandings but no epidemiological data. We found that our hidden variable modeling approach could successfully detect the per-capita effects of disease from monitored survival rates in both the experimental and wild populations. Our approach may prove useful for detecting epidemics from public health data in regions where standard surveillance techniques are not available and in the study of epidemics in wildlife populations, where longitudinal studies can be especially difficult to implement.

De novo genome assembly and genome skims reveal LTRs dominate the genome of a limestone endemic Mountainsnail (Oreohelix idahoensis).

BACKGROUND: Calcareous outcrops, rocky areas composed of calcium carbonate (CaCO3), often host a diverse, specialized, and threatened biomineralizing fauna. Despite the repeated evolution of physiological and morphological adaptations to colonize these mineral rich substrates, there is a lack of genomic resources for calcareous rock endemic species. This has hampered our ability to understand the genomic mechanisms underlying calcareous rock specialization and manage these threatened species. RESULTS: Here, we present a new draft genome assembly of the threatened limestone endemic land snail Oreohelix idahoensis and genome skim data for two other Oreohelix species. The O. idahoensis genome assembly (scaffold N50: 404.19 kb; 86.6% BUSCO genes) is the largest (~ 5.4 Gb) and most repetitive mollusc genome assembled to date (85.74% assembly size). The repetitive landscape was unusually dominated by an expansion of long terminal repeat (LTR) transposable elements (57.73% assembly size) which have shaped the evolution genome size, gene composition through retrotransposition of host genes, and ectopic recombination. Genome skims revealed repeat content is more than 2-3 fold higher in limestone endemic O. idahoensis compared to non-calcareous Oreohelix species. Gene family size analysis revealed stress and biomineralization genes have expanded significantly in the O. idahoensis genome. CONCLUSIONS: Hundreds of threatened land snail species are endemic to calcareous rock regions but there are very few genomic resources available to guide their conservation or determine the genomic architecture underlying CaCO3 resource specialization. Our study provides one of the first high quality draft genomes of a calcareous rock endemic land snail which will serve as a foundation for the conservation genomics of this threatened species and for other groups. The high proportion and activity of LTRs in the O. idahoensis genome is unprecedented in molluscan genomics and sheds new light how transposable element content can vary across molluscs. The genomic resources reported here will enable further studies of the genomic mechanisms underlying calcareous rock specialization and the evolution of transposable element content across molluscs.

A unified model of species abundance, genetic diversity, and functional diversity reveals the mechanisms structuring ecological communities.

Biodiversity accumulates hierarchically by means of ecological and evolutionary processes and feedbacks. Within ecological communities drift, dispersal, speciation, and selection operate simultaneously to shape patterns of biodiversity. Reconciling the relative importance of these is hindered by current models and inference methods, which tend to focus on a subset of processes and their resulting predictions. Here we introduce massive ecoevolutionary synthesis simulations (MESS), a unified mechanistic model of community assembly, rooted in classic island biogeography theory, which makes temporally explicit joint predictions across three biodiversity data axes: (i) species richness and abundances, (ii) population genetic diversities, and (iii) trait variation in a phylogenetic context. Using simulations we demonstrate that each data axis captures information at different timescales, and that integrating these axes enables discriminating among previously unidentifiable community assembly models. MESS is unique in generating predictions of community-scale genetic diversity, and in characterizing joint patterns of genetic diversity, abundance, and trait values. MESS unlocks the full potential for investigation of biodiversity processes using multidimensional community data including a genetic component, such as might be produced by contemporary eDNA or metabarcoding studies. We combine MESS with supervised machine learning to fit the parameters of the model to real data and infer processes underlying how biodiversity accumulates, using communities of tropical trees, arthropods, and gastropods as case studies that span a range of data availability scenarios, and spatial and taxonomic scales.

Phylogenetic diversity and community assembly in a naturally fragmented system.

We sought to assess effects of fragmentation and quantify the contribution of ecological processes to community assembly by measuring species richness, phylogenetic, and phenotypic diversity of species found in local and regional plant communities. Specifically, our fragmented system is Craters of the Moon National Monument and Preserve, Idaho, USA. CRMO is characterized by vegetated islands, kipukas, that are isolated in a matrix of lava. We used floristic surveys of vascular plants in 19 kipukas to create a local species list to compare traditional dispersion metrics, mean pairwise distance, and mean nearest taxon distance (MPD and MNTD), to a regional species list with phenotypic and phylogenetic data. We combined phylogenetic and functional trait data in a novel machine-learning model selection approach, Community Assembly Model Inference (CAMI), to infer probability associated with different models of community assembly given the data. Finally, we used linear regression to explore whether the geography of kipukas explained estimated support for community assembly models. Using traditional metrics of MPD and MNTD neutral processes received the most support when comparing kipuka species to regional species. Individually no kipukas showed significant support for overdispersion. Rather, five kipukas showed significant support for phylogenetic clustering using MPD and two kipukas using MNTD. Using CAMI, we inferred neutral and filtering models structured the kipuka plant community for our trait of interest. Finally, we found as species richness in kipukas increases, model support for competition decreases and lower elevation kipukas show more support for habitat filtering models. While traditional phylogenetic community approaches suggest neutral assembly dynamics, recently developed approaches utilizing machine learning and model choice revealed joint influences of assembly processes to form the kipuka plant communities. Understanding ecological processes at play in naturally fragmented systems will aid in guiding our understanding of how fragmentation impacts future changes in landscapes.

Polistes versicolor (Hymenoptera: Vespidae), an Introduced Wasp in the Galapagos Islands: Its Life Cycle and Ecological Impact.

The yellow paper wasp, Polistes versicolor (Olivier) was first recorded in the Galapagos archipelago in 1988. Its life cycle and ecological impacts were studied on two islands 11 yr after it was first discovered. This invasive wasp adapted quickly and was found in most environments. Colony counts and adult wasp monitoring showed a strong preference for drier habitats. Nest activities were seasonally synchronized, nest building followed the rains in the hot season (typically January-May), when insect prey increases, and peaked as temperature and rains started to decline. Next, the number of adult wasps peaked during the cool season when there is barely any rain in the drier zones. In Galapagos, almost half of the prey loads of P. versicolor were lepidopteran larvae, but wasps also carried spiders, beetles, and flies back to the colonies. An estimated average of 329 mg of fresh insect prey was consumed per day for an average colony of 120-150 wasp larvae. The wasps preyed upon native and introduced insects, but likely also affect insectivorous vertebrates as competitors for food. Wasps may also compete with native pollinators as they regularly visited flowers to collect nectar, and have been recorded visiting at least 93 plant species in Galapagos, including 66 endemic and native plants. Colonies were attacked by a predatory moth, Taygete sphecophila (Meyrick) (Lepidoptera: Autostichidae), but colony development was not arrested. High wasp numbers also affect the activities of residents and tourists. A management program for this invasive species in the archipelago is essential.

Comparing Adaptive Radiations Across Space, Time, and Taxa.

Adaptive radiation plays a fundamental role in our understanding of the evolutionary process. However, the concept has provoked strong and differing opinions concerning its definition and nature among researchers studying a wide diversity of systems. Here, we take a broad view of what constitutes an adaptive radiation, and seek to find commonalities among disparate examples, ranging from plants to invertebrate and vertebrate animals, and remote islands to lakes and continents, to better understand processes shared across adaptive radiations. We surveyed many groups to evaluate factors considered important in a large variety of species radiations. In each of these studies, ecological opportunity of some form is identified as a prerequisite for adaptive radiation. However, evolvability, which can be enhanced by hybridization between distantly related species, may play a role in seeding entire radiations. Within radiations, the processes that lead to speciation depend largely on (1) whether the primary drivers of ecological shifts are (a) external to the membership of the radiation itself (mostly divergent or disruptive ecological selection) or (b) due to competition within the radiation membership (interactions among members) subsequent to reproductive isolation in similar environments, and (2) the extent and timing of admixture. These differences translate into different patterns of species accumulation and subsequent patterns of diversity across an adaptive radiation. Adaptive radiations occur in an extraordinary diversity of different ways, and continue to provide rich data for a better understanding of the diversification of life.

Archipelago-Wide Patterns of Colonization and Speciation Among an Endemic Radiation of Galápagos Land Snails.

Newly arrived species on young or remote islands are likely to encounter less predation and competition than source populations on continental landmasses. The associated ecological release might facilitate divergence and speciation as colonizing lineages fill previously unoccupied niche space. Characterizing the sequence and timing of colonization on islands represents the first step in determining the relative contributions of geographical isolation and ecological factors in lineage diversification. Herein, we use genome-scale data to estimate timing of colonization in Naesiotus snails to the Galápagos islands from mainland South America. We test inter-island patterns of colonization and within-island radiations to understand their contribution to community assembly. Partly contradicting previously published topologies, phylogenetic reconstructions suggest that most Naesiotus species form island-specific clades, with within-island speciation dominating cladogenesis. Galápagos Naesiotus also adhere to the island progression rule, with colonization proceeding from old to young islands and within-island diversification occurring earlier on older islands. Our work provides a framework for evaluating the contribution of colonization and in situ speciation to the diversity of other Galápagos lineages.

Mitochondrial Genome Sequence of the Land Snail Oreohelix idahoensis.

We announce the complete mitochondrial genome sequence of Oreohelix idahoensis, a threatened land snail endemic to the Pacific Northwest of the United States. The circular genome is 14.2 kb and contains 13 protein-coding genes, 2 rRNA genes, and 21 tRNA genes.

Application of the Open qPCR Instrument for the in Vitro Selection of DNA Aptamers against Epidermal Growth Factor Receptor and Drosophila C Virus.

The low-cost Open qPCR instrument can be used for different tasks in the aptamer selection process: quantification of DNA, cycle course optimization, screening, and final binding characterization. We have selected aptamers against whole Drosophila C virus (DCV) particles and recombinant epidermal growth factor receptor (EGFR). We performed systematic evolution of ligands by exponential enrichment (SELEX) using the Open qPCR to optimize each amplification step. The Open qPCR instrument identified the best aptamer candidate. The Open qPCR has the capacity to perform melt curves, and we used this function to perform thermofluorimetric analysis (TFA) to quantify target-aptamer binding. We confirmed target-aptamer binding using flow cytometry. A sandwich type luminescence bioassay based on our anti-DCV aptamer was sensitive to DCV and did not respond to a related virus, demonstrating that our selected anti-DCV aptamer can be used to specifically detect DCV.

Convergent Phenotypic Evolution despite Contrasting Demographic Histories in the Fauna of White Sands.

When are evolutionary outcomes predictable? Cases of convergent evolution can shed light on when, why, and how different species exhibit shared evolutionary trajectories. In particular, studying diverse species in a common environment can illuminate how different factors facilitate or constrain adaptive evolution. Here we integrate studies of pattern and process in the fauna at White Sands (New Mexico) to understand the determinants of convergent evolution. Numerous animal species at White Sands exhibit phenotypic convergence in response to a novel-and shared-selective environment: geologically young gypsum dunes. We synthesize 15 years of research on White Sands lizards to assess the contribution of natural selection, genetic architecture, and population demography to patterns of phenotypic evolution. We also present new data for two species of White Sands arthropods, Ammobaenetes arenicolus and Habronattus ustulatus. Overall, we find dramatic phenotypic convergence across diverse species at White Sands. Although the direction of phenotypic response is parallel, the magnitude of phenotypic response varies among species. We also find that species exhibit strikingly different demographic patterns across the ecotone. The species with the most genetic structure between White Sands and dark-soil populations generally exhibit the least phenotypic divergence, suggesting population demography as a key modulator of adaptation. Comparative studies are particularly important for understanding the determinants of convergence in natural systems.

Mitochondrial Genome Sequence of the Galápagos Endemic Land Snail Naesiotus nux.

We report herein the draft mitochondrial genome sequence of Naesiotus nux, a Galápagos endemic land snail species of the genus Naesiotus. The circular genome is 15 kb and encodes 13 protein-coding genes, 2 rRNA genes, and 21 tRNA genes.

Intraspecific competition reduces niche width in experimental populations.

Intraspecific competition is believed to drive niche expansion, because otherwise suboptimal resources can provide a refuge from competition for preferred resources. Competitive niche expansion is well supported by empirical observations, experiments, and theory, and is often invoked to explain phenotypic diversification within populations, some forms of speciation, and adaptive radiation. However, some foraging models predict the opposite outcome, and it therefore remains unclear whether competition will promote or inhibit niche expansion. We conducted experiments to test whether competition changes the fitness landscape to favor niche expansion, and if competition indeed drives niche expansion as expected. Using Tribolium castaneum flour beetles fed either wheat (their ancestral resource), corn (a novel resource) or mixtures of both resources, we show that fitness is maximized on a mixed diet. Next, we show that at higher population density, the optimal diet shifts toward greater use of corn, favoring niche expansion. In stark contrast, when beetles were given a choice of resources, we found that competition caused niche contraction onto the ancestral resource. This presents a puzzling mismatch between how competition alters the fitness landscape, versus competition's effects on resource use. We discuss several explanations for this mismatch, highlighting potential reasons why optimality models might be misleading.

Strain diversity of Borrelia burgdorferi in ticks dispersed in North America by migratory birds.

The role of migratory birds in the dispersal of Ixodes scapularis ticks in the northeastern U.S. is well established and is presumed to be a major factor in the expansion of the geographic risk for Lyme disease. Population genetic studies of B. burgdorferi sensu stricto, the agent of Lyme disease in this region, consistently reveal the local presence of as many as 15 distinct strain types as designated by major groups of the ospC surface lipoprotein. Recent evidence suggests such strain diversity is adaptive to the diverse vertebrate hosts that maintain enzootic infection. How this strain diversity is established in emergent areas is unknown. To determine whether similar strain diversity is present in ticks imported by birds, we examined B. burgdorferi strains in I. scapularis ticks removed from migrants at an isolated island site. Tick mid-guts were cultured and isolates underwent DNA amplification with primers targeting ospC. Amplicons were separated by gel electrophoresis and sequenced. One hundred thirty-seven nymphal ticks obtained from 68 birds resulted in 24 isolates of B. burgdorferi representing eight ospC major groups. Bird-derived ticks contain diverse strain types of B. burgdorferi, including strain types associated with invasive Lyme disease. Birds and the ticks that feed on them may introduce a diversity of strains of the agent of Lyme disease to emergent areas.

Ecological opportunity in adaptive radiation of Galápagos endemic land snails.

The classic evolutionary hypothesis of ecological opportunity proposes that both heterogeneity of resources and freedom from enemies promote phenotypic divergence as a response to increased niche availability. Although phenotypic divergence and speciation have often been inferred to be the primary consequences of the release from competition or predation that accompanies a shift to a new adaptive zone, increased phenotypic variation within species is expected to represent the first stage resulting from such a shift. Using measures of intraspecific morphological variation of 30 species of Galápagos endemic land snails in a phylogenetically controlled framework, we show that the number of local congeners and the number of local plant species are associated with lower and higher intraspecific phenotypic variation, respectively. In this clade, ecological opportunity thus explicitly links the role of competition from congeners and the heterogeneity of resources to the extent of intraspecific phenotypic divergence as adaptive radiation proceeds.

Colonization and diversification of Galápagos terrestrial fauna: a phylogenetic and biogeographical synthesis.

Remote oceanic islands have long been recognized as natural models for the study of evolutionary processes involved in diversification. Their remoteness provides opportunities for isolation and divergence of populations, which make islands remarkable settings for the study of diversification. Groups of islands may share a relatively similar geological history and comparable climate, but their inhabitants experience subtly different environments and have distinct evolutionary histories, offering the potential for comparative studies. A range of organisms have colonized the Galápagos Islands, and various lineages have radiated throughout the archipelago to form unique assemblages. This review pays particular attention to molecular phylogenetic studies of Galápagos terrestrial fauna. We find that most of the Galápagos terrestrial fauna have diversified in parallel to the geological formation of the islands. Lineages have occasionally diversified within islands, and the clearest cases occur in taxa with very low vagility and on large islands with diverse habitats. Ecology and habitat specialization appear to be critical in speciation both within and between islands. Although the number of phylogenetic studies is continuously increasing, studies of natural history, ecology, evolution and behaviour are essential to completely reveal how diversification proceeded on these islands.

Sequential colonization and diversification of Galapágos endemic land snail genus Bulimulus (Gastropoda, Stylommatophora).

Species richness on island or islandlike systems is a function of colonization, within-island speciation, and extinction. Here we evaluate the relative importance of the first two of these processes as a function of the biogeographical and ecological attributes of islands using the Galápagos endemic land snails of the genus Bulimulus, the most species-rich radiation of these islands. Species in this clade have colonized almost all major islands and are found in five of the six described vegetation zones. We use molecular phylogenetics (based on COI and ITS 1 sequence data) to infer the diversification patterns of extant species of Bulimulus, and multiple regression to investigate the causes of variation among islands in species richness. Maximum-likelihood, Bayesian, and maximum-parsimony analyses yield well-resolved trees with similar topologies. The phylogeny obtained supports the progression rule hypothesis, with species found on older emerged islands connecting at deeper nodes. For all but two island species assemblages we find support for only one or two colonization events, indicating that within-island speciation has an important role in the formation of species on these islands. Even though speciation through colonization is not common, island insularity (distance to nearest major island) is a significant predictor of species richness resulting from interisland colonization alone. However, island insularity has no effect on the overall bulimulid species richness per island. Habitat diversity (measured as plant species diversity), island elevation, and island area, all of which are indirect measures of niche space, are strong predictors of overall bulimulid land snail species richness. Island age is also an important independent predictor of overall species richness, with older islands harboring more species than younger islands. Taken together, our results demonstrate that the diversification of Galápagos bulimulid land snails has been driven by a combination of geographic factors (island age, size, and location), which affect colonization patterns, and ecological factors, such as plant species diversity, that foster within-island speciation.