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.

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.

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.

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.