Changes in capture availability due to infection can lead to detectable biases in population-level infectious disease parameters.

Correctly identifying the strength of selection that parasites impose on hosts is key to predicting epidemiological and evolutionary outcomes of host-parasite interactions. However, behavioral changes due to infection can alter the capture probability of infected hosts and thereby make selection difficult to estimate by standard sampling techniques. Mark-recapture approaches, which allow researchers to determine if some groups in a population are less likely to be captured than others, can be used to identify infection-driven capture biases. If a metric of interest directly compares infected and uninfected populations, calculated detection probabilities for both groups may be useful in identifying bias. Here, we use an individual-based simulation to test whether changes in capture rate due to infection can alter estimates of three key metrics: 1) reduction in the reproductive success of infected parents relative to uninfected parents, 2) the relative risk of infection for susceptible genotypes compared to resistant genotypes, and 3) changes in allele frequencies between generations. We explore the direction and underlying causes of the biases that emerge from these simulations. Finally, we argue that short series of mark-recapture sampling bouts, potentially implemented in under a week, can yield key data on detection bias due to infection while not adding a significantly higher burden to disease ecology studies.

Parsing variance by marker type: Testing biogeographic hypotheses and differential contribution of historical processes to population structure in a desert lizard.

A fundamental goal of population genetic studies is to identify historical biogeographic patterns and understand the processes that generate them. However, localized demographic events can skew population genetic inference. Assessing populations with multiple types of genetic markers, each with unique mutation rates and responses to changes in population size, can help to identify potentially confounding population-specific demographic processes. Here, we compared population structure and connectivity inferred from microsatellites and restriction site-associated DNA loci among 17 populations of an arid-specialist lizard, the desert night lizard, Xantusia vigilis, in central California to test among historical processes structuring population genetic diversity. We found that both marker types yielded generally concordant insights into population genetic structure including a major phylogenetic break maintained between two populations separated by less than 10 km, suggesting that either marker type could be used to understand generalized demographic patterns across the region for management purposes. However, we also found that the effects of demography on marker discordance could be used to elucidate population histories and distinguish among competing biogeographic hypotheses. Our results suggest that comparisons of within-population diversity across marker types provide powerful opportunities for leveraging marker discordance, particularly for understanding the creation and maintenance of contact zones among clades.

Phylogenetically under-dispersed gut microbiomes are not correlated with host genomic heterozygosity in a genetically diverse reptile community.

While key elements of fitness in vertebrate animals are impacted by their microbiomes, the host genetic characteristics that factor into microbiome composition are not fully understood. Here, we correlate host genomic heterozygosity and gut microbiome phylogenetic diversity across a community of reptiles in southwestern New Mexico to test hypotheses about the behaviour of host genes that drive microbiome assembly. We find that microbiome communities are phylogenetically under-dispersed relative to random expectations, and that host heterozygosity is not correlated with microbiome diversity. Our analyses reinforce results from functional genomic work that identify conserved host immune and nonimmune genes as key players in microbiome assembly, rather than gene families that rely on heterozygosity for their function.

Assembling microbial communities: a genomic analysis of a natural experiment in neotropical bamboo internodes.

Microbes participate in ecological communities, much like multicellular organisms. However, microbial communities lack the centuries of observation and theory describing and predicting ecological processes available for multicellular organisms. Here, we examine early bacterial community assembly in the water-filled internodes of Amazonian bamboos from the genus Guadua. Bamboo stands form distinct habitat patches within the lowland Amazonian rainforest and provide habitat for a suite of vertebrate and invertebrate species. Guadua bamboos develop sealed, water-filled internodes as they grow. Internodes are presumed sterile or near sterile while closed, but most are eventually opened to the environment by animals, after which they are colonized by microbes. We find that microbial community diversity increases sharply over the first few days of environmental exposure, and taxonomic identity of the microbes changes through this time period as is predicted for early community assembly in macroscopic communities. Microbial community taxonomic turnover is consistent at the bacteria phylum level, but at the level of Operational Taxonomic Units (OTUs), internode communities become increasingly differentiated through time. We argue that these tropical bamboos form an ideal study system for microbial community ecology due to their near-sterile condition prior to opening, relatively consistent environment after opening, and functionally limitless possibilities for replicates. Given the possible importance of opened internode habitats as locations of transmission for both pathogenic and beneficial microbes among animals, understanding the microbial dynamics of the internode habitat is a key conservation concern for the insect and amphibian species that use this microhabitat.

Genetic mechanisms and correlational selection structure trait variation in a coral snake mimic.

Covariation among traits shapes both phenotypic evolution and ecological interactions across space and time. However, rampant geographical variation in the strength and direction of such correlations can be particularly difficult to explain through generalized mechanisms. By integrating population genomics, surveys of natural history collections and spatially explicit analyses, we tested multiple drivers of trait correlations in a coral snake mimic that exhibits remarkable polymorphism in mimetic and non-mimetic colour traits. We found that although such traits co-occur extensively across space, correlations were best explained by a mixture of genetic architecture and correlational selection, rather than by any single mechanism. Our findings suggest that spatially complex trait distributions may be driven more by the simple interaction between multiple processes than by complex variation in one mechanism alone. These interactions are particularly important in mimicry systems, which frequently generate striking geographical variation and genetic correlations among colour pattern traits.

Metabolically similar cohorts of bacteria exhibit strong cooccurrence patterns with diet items and eukaryotic microbes in lizard guts.

Gut microbiomes perform essential services for their hosts, including helping them to digest food and manage pathogens and parasites. Performing these services requires a diverse and constantly changing set of metabolic functions from the bacteria in the microbiome. The metabolic repertoire of the microbiome is ultimately dependent on the outcomes of the ecological interactions of its member microbes, as these interactions in part determine the taxonomic composition of the microbiome. The ecological processes that underpin the microbiome's ability to handle a variety of metabolic challenges might involve rapid turnover of the gut microbiome in response to new metabolic challenges, or it might entail maintaining sufficient diversity in the microbiome that any new metabolic demands can be met from an existing set of bacteria. To differentiate between these scenarios, we examine the gut bacteria and resident eukaryotes of two generalist-insectivore lizards, while simultaneously identifying the arthropod prey each lizard was digesting at the time of sampling. We find that the cohorts of bacteria that occur significantly more or less often than expected with arthropod diet items or eukaryotes include bacterial species that are highly similar to each other metabolically. This pattern in the bacterial microbiome could represent an early step in the taxonomic shifts in bacterial microbiome that occur when host lineages change their diet niche over evolutionary timescales.

Widespread chytrid infection across frogs in the Peruvian Amazon suggests critical role for low elevation in pathogen spread and persistence.

Outbreaks of emerging infectious diseases are becoming more frequent as climate changes wildlife communities at unprecedented rates, driving population declines and raising concerns for species conservation. One critical disease is the global pandemic of chytridiomycosis in frogs, which can be caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd). Although there is clear evidence for Bd-induced mortality across high-elevation frog communities, little attention is given to the role of lowlands in Bd's persistence and spread because low elevations are assumed to be too warm to harbor significant levels of Bd. Here, we report widespread Bd infection across 80 frog species from three sites in the lowland Peruvian Amazon, an area with no documented Bd-related amphibian declines. Despite observing no clinical signs of infection in the field, we found that 24-46% of individuals were infected per site (up to ≈105,000 zoospore equivalents per frog) by three Bd strains from the global pandemic lineage (Bd-GPL). We also found collection site and seasonal effects to be only weak predictors of Bd prevalence and load, with lower elevation and drier habitats marginally decreasing both prevalence and load. We found no further effect of host phylogeny, ecotype, or body size. Our results showing high and widespread prevalence across a lowland tropical ecosystem contradict the expectations based on the global pattern of pathogenicity of Bd that is largely restricted to higher elevations and colder temperatures. These findings imply that the lowlands may play a critical role in the spread and persistence of Bd over time and space.

Does Population Structure Predict the Rate of Speciation? A Comparative Test across Australia's Most Diverse Vertebrate Radiation.

Population divergence is the first step in allopatric speciation, as has long been recognized in both theoretical models of speciation and empirical explorations of natural systems. All else being equal, lineages with substantial population differentiation should form new species more quickly than lineages that maintain range-wide genetic cohesion through high levels of gene flow. However, there have been few direct tests of the extent to which population differentiation predicts speciation rates as measured on phylogenetic trees. Here, we explicitly test the links between organismal traits, population-level processes, and phylogenetic speciation rates across a diverse clade of Australian lizards that shows remarkable variation in speciation rate. Using genome-wide double digest restriction site-associated DNA data from 892 individuals, we generated a comparative data set on isolation by distance and population differentiation across 104 putative species-level lineages (operational taxonomic units). We find that species show substantial variation in the extent of population differentiation, and this variation is predicted by organismal traits that are thought to be proxies for dispersal and deme size. However, variation in population structure does not predict variation in speciation rate. Our results suggest that population differentiation is not the rate-limiting step in species formation and that other ecological and historical factors are primary determinants of speciation rates at macroevolutionary scales.

Natural history bycatch: a pipeline for identifying metagenomic sequences in RADseq data.

BACKGROUND: Reduced representation genomic datasets are increasingly becoming available from a variety of organisms. These datasets do not target specific genes, and so may contain sequences from parasites and other organisms present in the target tissue sample. In this paper, we demonstrate that (1) RADseq datasets can be used for exploratory analysis of tissue-specific metagenomes, and (2) tissue collections house complete metagenomic communities, which can be investigated and quantified by a variety of techniques. METHODS: We present an exploratory method for mining metagenomic "bycatch" sequences from a range of host tissue types. We use a combination of the pyRAD assembly pipeline, NCBI's blastn software, and custom R scripts to isolate metagenomic sequences from RADseq type datasets. RESULTS: When we focus on sequences that align with existing references in NCBI's GenBank, we find that between three and five percent of identifiable double-digest restriction site associated DNA (ddRAD) sequences from host tissue samples are from phyla to contain known blood parasites. In addition to tissue samples, we examine ddRAD sequences from metagenomic DNA extracted snake and lizard hind-gut samples. We find that the sequences recovered from these samples match with expected bacterial and eukaryotic gut microbiome phyla. DISCUSSION: Our results suggest that (1) museum tissue banks originally collected for host DNA archiving are also preserving valuable parasite and microbiome communities, (2) that publicly available RADseq datasets may include metagenomic sequences that could be explored, and (3) that restriction site approaches are a useful exploratory technique to identify microbiome lineages that could be missed by primer-based approaches.

Predator Perspective Drives Geographic Variation in Frequency-Dependent Polymorphism.

Color polymorphism in natural populations can manifest as a striking patchwork of phenotypes in space, with neighboring populations characterized by dramatic differences in morph composition. These geographic mosaics can be challenging to explain in the absence of localized selection because they are unlikely to result from simple isolation-by-distance or clinal variation in selective regimes. To identify processes that can lead to the formation of geographic mosaics, we developed a simulation-based model to explore the influence of predator perspective, selection, migration, and genetic linkage of color loci on allele frequencies in polymorphic populations over space and time. Using simulated populations inspired by the biology of Heliconius longwing butterflies, Cepaea land snails, Oophaga poison frogs, and Sonora ground snakes, we found that the relative sizes of predator and prey home ranges can produce large differences in morph composition between neighboring populations under both positive and negative frequency-dependent selection. We also demonstrated the importance of the interaction of predator perspective with the type of frequency dependence and localized directional selection across migration and selection intensities. Our results show that regional-scale predation can promote the formation of phenotypic mosaics in prey species, without the need to invoke spatial variation in selective regimes. We suggest that predator behavior can play an important and underappreciated role in the formation and maintenance of geographic mosaics in polymorphic species.

Genetic diversity is largely unpredictable but scales with museum occurrences in a species-rich clade of Australian lizards.

Genetic diversity is a fundamental characteristic of species and is affected by many factors, including mutation rate, population size, life history and demography. To better understand the processes that influence levels of genetic diversity across taxa, we collected genome-wide restriction-associated DNA data from more than 500 individuals spanning 76 nominal species of Australian scincid lizards in the genus Ctenotus To avoid potential biases associated with variation in taxonomic practice across the group, we used coalescent-based species delimitation to delineate 83 species-level lineages within the genus for downstream analyses. We then used these genetic data to infer levels of within-population genetic diversity. Using a phylogenetically informed approach, we tested whether variation in genetic diversity could be explained by population size, environmental heterogeneity or historical demography. We find that the strongest predictor of genetic diversity is a novel proxy for census population size: the number of vouchered occurrences in museum databases. However, museum occurrences only explain a limited proportion of the variance in genetic diversity, suggesting that genetic diversity might be difficult to predict at shallower phylogenetic scales.

Historical Environment Is Reflected in Modern Population Genetics and Biogeography of an Island Endemic Lizard (Xantusia riversiana reticulata).

The restricted distribution and isolation of island endemics often produces unique genetic and phenotypic diversity of conservation interest to management agencies. However, these isolated species, especially those with sensitive life history traits, are at high risk for the adverse effects of genetic drift and habitat degradation by non-native wildlife. Here, we study the population genetic diversity, structure, and stability of a classic "island giant" (Xantusia riversiana, the Island Night Lizard) on San Clemente Island, California following the removal of feral goats. Using DNA microsatellites, we found that this population is reasonably genetically robust despite historical grazing, with similar effective population sizes and genetic diversity metrics across all sampling locations irrespective of habitat type and degree of degradation. However, we also found strong site-specific patterns of genetic variation and low genetic diversity compared to mainland congeners, warranting continued special management as an island endemic. We identify both high and low elevation areas that remain valuable repositories of genetic diversity and provide a case study for other low-dispersal coastal organisms in the face of future climate change.

Coral snakes predict the evolution of mimicry across New World snakes.

Batesian mimicry, in which harmless species (mimics) deter predators by deceitfully imitating the warning signals of noxious species (models), generates striking cases of phenotypic convergence that are classic examples of evolution by natural selection. However, mimicry of venomous coral snakes has remained controversial because of unresolved conflict between the predictions of mimicry theory and empirical patterns in the distribution and abundance of snakes. Here we integrate distributional, phenotypic and phylogenetic data across all New World snake species to demonstrate that shifts to mimetic coloration in nonvenomous snakes are highly correlated with coral snakes in both space and time, providing overwhelming support for Batesian mimicry. We also find that bidirectional transitions between mimetic and cryptic coloration are unexpectedly frequent over both long- and short-time scales, challenging traditional views of mimicry as a stable evolutionary 'end point' and suggesting that insect and snake mimicry may have different evolutionary dynamics.

Temporal population genetic instability in range-edge western toads, Anaxyrus boreas.

In this article, we address the temporal stability of population genetic structure in a range-edge population that is undergoing continual, short-distance colonization events. We sampled western toad, Anaxyrus boreas, breeding populations over 2 seasons near their northern range limit in southeast Alaska. We sampled 20 ponds each during the summers of 2008 and 2009, with 14 ponds sampled in both summers. We found considerable turnover in the population genetic relationships among ponds in those 2 seasons, as well as biologically meaningful genetic differentiation between years within some ponds. We found relatively consistent relationships between major population centers, whereas the relationships between the central ponds and smaller, outlying populations differed year to year. This finding indicates that multiple years of genetic sampling may be important for understanding the genetic landscape of some populations.