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The role of neutral and adaptive genomic variation in population diversification and speciation in two ground squirrel species of conservation concern

Understanding the neutral (demographic) and adaptive processes leading to the differentiation of species and populations is a critical component of evolutionary and conservation biology. In this context, recently diverged taxa represent a unique opportunity to study the process of genetic differentiation. Northern and southern Idaho ground squirrels ( Urocitellus brunneus —NIDGS, and U . endemicus —SIDGS, respectively) are a recently diverged pair of sister species that have undergone dramatic declines in the last 50 years and are currently found in metapopulations across restricted spatial areas with distinct environmental pressures. Here we genotyped single-nucleotide polymorphisms (SNPs) from buccal swabs with restriction site-associated DNA sequencing (RADseq). With these data we evaluated neutral genetic structure at both the inter- and intraspecific level, and identified putatively adaptive SNPs using population structure outlier detection and genotype–environment association (GEA) analyses. At the interspecific level, we detected a clear separation between NIDGS and SIDGS, and evidence for adaptive differentiation putatively linked to torpor patterns. At the intraspecific level, we found evidence of both neutral and adaptive differentiation. For NIDGS, elevation appears to be the main driver of adaptive differentiation, while neutral variation patterns match and expand information on the low connectivity between some populations identified in previous studies using microsatellite markers. For SIDGS, neutral substructure generally reflected natural geographical barriers, while adaptive variation reflected differences in land cover and temperature, as well as elevation. These results clearly highlight the roles of neutral and adaptive processes for understanding the complexity of the processes leading to species and population differentiation, which can have important conservation implications in susceptible and threatened species.

Idaho

Dispersive currents explain patterns of population connectivity in an ecologically and economically important fish

How to identify the drivers of population connectivity remains a fundamental question in ecology and evolution. Answering this question can be challenging in aquatic environments where dynamic lake and ocean currents coupled with high levels of dispersal and gene flow can decrease the utility of modern population genetic tools. To address this challenge, we used RAD-Seq to genotype 959 yellow perch ( Perca flavescens ), a species with an ~40-day pelagic larval duration (PLD), collected from 20 sites circumscribing Lake Michigan. We also developed a novel, integrative approach that couples detailed biophysical models with eco-genetic agent-based models to generate “predictive” values of genetic differentiation. By comparing predictive and empirical values of genetic differentiation, we estimated the relative contributions for known drivers of population connectivity (e.g., currents, behavior, PLD). For the main basin populations (i.e., the largest contiguous portion of the lake), we found that high gene flow led to low overall levels of genetic differentiation among populations ( F ST = 0.003). By far the best predictors of genetic differentiation were connectivity matrices that were derived from periods of time when there were strong and highly dispersive currents. Thus, these highly dispersive currents are driving the patterns of population connectivity in the main basin. We also found that populations from the northern and southern main basin are slightly divergent from one another, while those from Green Bay and the main basin are highly divergent ( F ST = 0.11). By integrating biophysical and eco-genetic models with genome-wide data, we illustrate that the drivers of population connectivity can be identified in high gene flow systems.

Lake Michigan

Multiple estimates of effective population size for monitoring a long-lived vertebrate: An application to Yellowstone grizzly bears

Effective population size ( N e ) is a key parameter for monitoring the genetic health of threatened populations because it reflects a population's evolutionary potential and risk of extinction due to genetic stochasticity. However, its application to wildlife monitoring has been limited because it is difficult to measure in natural populations. The isolated and well-studied population of grizzly bears ( Ursus arctos ) in the Greater Yellowstone Ecosystem provides a rare opportunity to examine the usefulness of different N e estimators for monitoring. We genotyped 729 Yellowstone grizzly bears using 20 microsatellites and applied three single-sample estimators to examine contemporary trends in generation interval (GI), effective number of breeders ( N b ) and N e during 1982–2007. We also used multisample methods to estimate variance ( N eV ) and inbreeding N e ( N eI ). Single-sample estimates revealed positive trajectories, with over a fourfold increase in N e (≈100 to 450) and near doubling of the GI (≈8 to 14) from the 1980s to 2000s. N eV (240–319) and N eI (256) were comparable with the harmonic mean single-sample N e (213) over the time period. Reanalysing historical data, we found N eV increased from ≈80 in the 1910s–1960s to ≈280 in the contemporary population. The estimated ratio of effective to total census size ( N e /N c ) was stable and high (0.42–0.66) compared to previous brown bear studies. These results support independent demographic evidence for Yellowstone grizzly bear population growth since the 1980s. They further demonstrate how genetic monitoring of N e can complement demographic-based monitoring of N c and vital rates, providing a valuable tool for wildlife managers.

Idaho, Montana, Wyoming

Nest structure affects auditory and visual detectability, but not predation risk, in a tropical songbird community

Offspring mortality varies dramatically among species with critical demographic and evolutionary ramifications, yet the causes of this variation remain unclear. Nests are widely used for breeding across taxa and thought to influence offspring mortality risk. Traditionally, more complex, enclosed nest structures are thought to reduce offspring predation by reducing the visibility of nest contents and muffling offspring sounds compared to open nests. Direct tests of the functional bases for nest structure influence on predation risk are lacking. We used experiments and 10 years of observational data to examine how nest structure influences nest predation risk in a diverse community of tropical songbirds. First, we examined how nest size was related to nest structure and nest predation rates across species. Second, we assessed how nest structure influences the detectability of nestling begging calls both in field and in laboratory settings. Finally, we examined how the acoustic properties of different nest structures influence nest predation risk. Specifically, we experimentally broadcast begging calls from open and enclosed nests to determine how auditory cues and nest structure interact to affect predation on plasticine and quail eggs. We also tested whether nest structure was associated with differences in nest predation rates between the incubation (no begging cues) and nestling (begging cues) stages. We found that enclosed nests are larger than open nests after accounting for adult size, and larger nests had increased predation rates. Moreover, enclosed nests did not consistently alter nestling begging calls in ways that reduce the likelihood of predation compared to open nests. Indeed, begging cues increased predation rates for enclosed but not open‐cup nests in our playback experiment, and nest predation rates showed greater increases after hatching in enclosed than open‐cup nests. Ultimately, enclosed nests do not necessarily provide greater predation benefits than open nests in contrast to long‐standing theory.

Functional Ecology

Conditions favouring Bromus tectorum dominance of endangered sagebrush steppe ecosystems

1. Ecosystem invasibility is determined by combinations of environmental variables, invader attributes, disturbance regimes, competitive abilities of resident species and evolutionary history between residents and disturbance regimes. Understanding the relative importance of each factor is critical to limiting future invasions and restoring ecosystems. 2. We investigated factors potentially controlling Bromus tectorum invasions into Artemisia tridentata ssp. wyomingensis communities across 75 sites in the Great Basin. We measured soil texture, cattle grazing intensity, gaps among perennial plants and plant cover including B. tectorum, biological soil crusts (BSCs) and bare soil. Using a priori knowledge, we developed a multivariate hypothesis of the susceptibility of Artemisia ecosystems to B. tectorum invasion and used the model to assess the relative importance of the factors driving the magnitude of such invasions. 3. Model results imply that bunchgrass community structure, abundance and composition, along with BSC cover, play important roles in controlling B. tectorum dominance. Evidence suggests abundant bunchgrasses limit invasions by limiting the size and connectivity of gaps between vegetation, and BSCs appear to limit invasions within gaps. Results also suggest that cattle grazing reduces invasion resistance by decreasing bunchgrass abundance, shifting bunchgrass composition, and thereby increasing connectivity of gaps between perennial plants while trampling further reduces resistance by reducing BSC. 4. Synthesis and applications. Grazing exacerbates Bromus tectorum dominance in one of North America's most endangered ecosystems by adversely impacting key mechanisms mediating resistance to invasion. If the goal is to conserve and restore resistance of these systems, managers should consider maintaining or restoring: (i) high bunchgrass cover and structure characterized by spatially dispersed bunchgrasses and small gaps between them; (ii) a diverse assemblage of bunchgrass species to maximize competitive interactions with B. tectorum in time and space; and (iii) biological soil crusts to limit B. tectorum establishment. Passive restoration by reducing cumulative cattle grazing may be one of the most effective means of achieving these three goals.

Journal of Applied Ecology

Host vs. pathogen evolutionary arms race: Effects of exposure history on individual response to a genetically diverse pathogen

Introduction: Throughout their range, bighorn sheep ( Ovis canadensis ) populations have seen significant disease-associated declines. Unfortunately, understanding of the underlying epidemiological processes driving the disease dynamics in this species has hindered conservation efforts aimed at improving the health and long-term viability of these populations. Individual response to pathogen exposure emerges from dynamic interactions between competing evolutionary processes within the host and pathogen. The host’s adaptive immune system recognizes pathogens and mounts a defensive response. Pathogens have evolved strategies to overcome adaptive immune defenses including maintaining high genetic diversity through rapid evolution. The outcomes of this evolutionary warfare determine the success of pathogen invasion of the host and ultimately the success of conservation efforts. Methods: During an epizootic dominated by a single strain, we explore these host-pathogen dynamics by examining the variation in effects of pathogen invasion on captive bighorn sheep with differing histories of exposure to genetically diverse strains of Mycoplasma ovipneumoniae (Movi). We monitored clinical signs of disease and sampled animals and their environment to detect spread of Movi among 37 bighorn sheep separated into nine pens based on known exposure Results: We documented Movi transmission within and across pens and we detected Movi DNA in air, water, and invertebrate samples. Higher levels of antibody to Movi prior to the epizootic were associated with a lower likelihood of presenting clinical signs of pneumonia. Nonetheless, higher antibody levels in symptomatic individuals were associated with more severe progressive disease, increased probability and speed of pneumonia-induced mortality, and reduced likelihood of returning to a healthy state. Bighorn sheep with previous exposure to a strain other than the predominant epizootic strain were more likely to recover. Discussion: Our results indicate that Movi-strain variability was sufficient to overwhelm the adaptive host immunological defenses. This outcome indicates, in free-ranging herds, past exposure is likely insufficient to protect bighorn sheep from infection by new Movi strains, although it influences the progression of disease and recovery within the herd. Therefore, given Movi-strain variability and the lack of immunological protection from past exposure, focusing management efforts on minimizing the introduction of Movi into bighorn herds, through separation of domestic and bighorn sheep and avoidance of management activities that create commingling of bighorn sheep carrying differing Movi strains, will likely be the most effective approach for reducing the effects of disease and achieving bighorn sheep conservation goals.

Idaho, Oregon, South Dakota, Washington

Considerations for maximizing the adaptive potential of restored coral populations in the western Atlantic

Active coral restoration typically involves two interventions: crossing gametes to facilitate sexual larval propagation; and fragmenting, growing, and outplanting adult colonies to enhance asexual propagation. From an evolutionary perspective, the goal of these efforts is to establish self‐sustaining, sexually reproducing coral populations that have sufficient genetic and phenotypic variation to adapt to changing environments. Here, we provide concrete guidelines to help restoration practitioners meet this goal for most Caribbean species of interest. To enable the persistence of coral populations exposed to severe selection pressure from many stressors, a mixed provenance strategy is suggested: genetically unique colonies (genets) should be sourced both locally as well as from more distant, environmentally distinct sites. Sourcing three to four genets per reef along environmental gradients should be sufficient to capture a majority of intraspecies genetic diversity. It is best for practitioners to propagate genets with one or more phenotypic traits that are predicted to be valuable in the future, such as low partial mortality, high wound healing rate, high skeletal growth rate, bleaching resilience, infectious disease resilience, and high sexual reproductive output. Some effort should also be reserved for underperforming genets because colonies that grow poorly in nurseries sometimes thrive once returned to the reef and may harbor genetic variants with as yet unrecognized value. Outplants should be clustered in groups of four to six genets to enable successful fertilization upon maturation. Current evidence indicates that translocating genets among distant reefs is unlikely to be problematic from a population genetic perspective but will likely provide substantial adaptive benefits. Similarly, inbreeding depression is not a concern given that current practices only raise first‐generation offspring. Thus, proceeding with the proposed management strategies even in the absence of a detailed population genetic analysis of the focal species at sites targeted for restoration is the best course of action. These basic guidelines should help maximize the adaptive potential of reef‐building corals facing a rapidly changing environment.

Ecological Applications

Mate fidelity improves survival and breeding propensity of a long‐lived bird

Evolutionary and behavioural ecologists have long been interested in factors shaping the variation in mating behaviour observed in nature. Although much of the research on this topic has focused on the consequences of mate choice and mate change on annual reproductive success, studies of a potential positive link between mate fidelity and adult demographic rates have been comparatively rare. This is particularly true for long‐lived birds with multi‐year, socially monogamous pair bonds. We used a 26‐year capture–mark–recapture dataset of 3,330 black brent Branta bernicla nigricans to test whether breeding with a familiar mate improved future breeding propensity and survival. We predicted that experienced breeders nesting with a new partner would have rates of survival similar to familiar pairs because long‐lived species avoid jeopardizing survival since their lifetime fitness is sensitive to this vital rate. In contrast, we expected that any costs of breeding with a new partner would be paid through skipping the subsequent breeding attempt. We found that unfamiliar pairs had lower subsequent breeding propensity than faithful partners. However, contrary to our expectations, individuals breeding with a new mate also suffered reduced survival. These results add to a small number of studies indicating that a positive relationship between mate retention and adult demographic rates may exist in a diverse array of avian species. Given these results, researchers should consider costs of mate change that extend beyond within‐season reproductive success to fully understand the potential adaptive basis for perennial social monogamy. We caution that if mate retention enhances survival prospects, improvements in annual reproductive success with pair‐bond length could be a secondary factor favouring perennial social monogamy, particularly in species with slower life‐history strategies. Furthermore, some cases where annual reproductive success does not improve with pair‐bond duration, yet multi‐year pair bonds are common, could be explained by benefits afforded by mate fidelity to adult vital rates.

Journal of Animal Ecology

Mechanisms associated with an advance in the timing of seasonal reproduction in an urban songbird

The colonization of urban environments by animals is often accompanied by earlier breeding and associated changes in seasonal schedules. Accelerated timing of seasonal reproduction in derived urban populations is a potential cause of evolutionary divergence from ancestral populations if differences in physiological processes that regulate reproductive timing become fixed over time. We compared reproductive development in free-living and captive male dark-eyed juncos deriving from a population that recently colonized a city (~35 years) and ceased migrating to that of conspecifics that live in sympatry with the urban population during winter and spring but migrate elsewhere to breed. We predicted that the earlier breeding sedentary urban birds would exhibit accelerated reproductive development in the spring along the hypothalamic-pituitary-gonadal (HPG) axis as compared to migrants. We found that free-living sedentary urban and migrant juncos differed at the level of the pituitary when measured as baseline luteinizing hormone (LH) levels, but not in increased LH when challenged with Gonadotropin-Releasing Hormone (GnRH). Among captives held in a common garden, and at the level of the gonad, we found that sedentary urban birds produced more testosterone in response to GnRH than migrants living in the same common environment, suggesting greater gonadal sensitivity in the derived urban population. Greater gonadal sensitivity could arise from greater upstream activation by LH or FSH or from reduced suppression of gonadal development by the adrenal axis. We compared abundance of gonadal transcripts for LH receptor (LHR), follicle stimulating hormone receptor (FSHR), glucocorticoid receptor (GR), and mineralocorticoid receptor (MR) in the common-garden, predicting either more abundant transcripts for LHR and FSHR or fewer transcripts for GR and MR in the earlier breeding sedentary urban breeders, as compared to the migrants. We found no difference in the expression of these genes. Together these data suggest that advanced timing of reproduction in a recently derived urban population is facilitated by earlier increase in upstream baseline activity of the HPG and earlier release from gonadal suppression by yet-to-be-discovered mechanisms. Evolutionarily, our results suggest that potential for gene flow between seasonally sympatric populations may be limited due to urban-induced advances in the timing of reproduction and resulting allochrony with ancestral forms.

California