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opencc-zeroNov 2020View details →

Supplemental data for article: DNA content variation and SNP diversity within a single population of asexual snails

A growing body of research suggests that many clonal populations maintain genetic diversity even without occasional sexual reproduction. The purpose of our study was to document variation in SNP diversity, DNA content, and pathogen susceptibility in clonal lineages of the New Zealand freshwater snail, Potamopyrgus antipodarum. We studied snails that were collected from multiple field sites around a single lake (Lake Alexandrina), as well as isofemale clonal lineages that had been isolated and maintained in the laboratory. We used the KASP method to genotype our samples at 46 nuclear SNP sites, and we used flow cytometry to estimate DNA content. We found high levels of SNP diversity, both in our field samples and in our clonal laboratory lines. We also found evidence of high variation in DNA content among clones, even among clones with identical genotypes across all SNP sites. Controlled pathogen exposures of the laboratory populations revealed variation in susceptibility among distinct clonal genotypes, which was independent of DNA content. Taken together, these results show high levels of diversity among asexual snails, especially for DNA content, and they suggest rapid genome evolution in asexuals.

opencc-zeroDec 2020View details →

Ancestral genetic variation in phenotypic plasticity underlies rapid evolutionary changes in resurrected populations of waterfleas

The role that phenotypic plasticity plays in adaptive evolution has been debated for decades. This is because the strength of natural selection is dependent upon the direction and magnitude of phenotypic responses to environmental signals. Therefore, the connection between plasticity and adaptation will depend on the patterns of plasticity harbored by ancestral populations prior to a change in the environment. Yet, few studies have directly assessed ancestral variation in plasticity and tracked phenotypic changes over time. Here we resurrected historic propagules of Daphnia spanning multiple species and lakes in Wisconsin following the invasion and proliferation of a novel predator (spiny waterflea, Bythotrephes longimanus). This approach revealed extensive genetic variation in predator-induced plasticity in ancestral populations of Daphnia. It is unlikely that the standing patterns of plasticity shielded Daphnia from selection to permit long-term coexistence with a novel predator. Instead, this variation in plasticity provided the raw materials for Bythotrephes-mediated selection to drive rapid shifts in Daphnia behavior and life history. Surprisingly, there was little evidence for the evolution of trait plasticity as genetic variation in plasticity was maintained in the face of a novel predator. Such results provide new insights into the link between plasticity and adaptation and highlight the importance of quantifying genetic variation in plasticity when evaluating the drivers of evolutionary change in the wild.

opencc-zeroFeb 2021View details →

Standing genetic variation in laboratory populations of insecticide-susceptible Phlebotomus papatasi and Lutzomyia longipalpis (Diptera: Psychodidae: Phlebotominae) for the evolution of resistance

Insecticides can exert strong selection on insect pest species, including those that vector diseases, and have led to rapid evolution of resistance. Despite such rapid evolution, relatively little is known about standing genetic variation for resistance in insecticide-susceptible populations of many species. To help fill this knowledge gap, we generated genotyping-by-sequencing data from insecticide-susceptible Phlebotomus papatasi and Lutzomyia longipalpis sand flies that survived or died from a sub-diagnostic exposure to either permethrin or malathion using a modified version of the Centers for Disease Control and Prevention bottle bioassay. Multi-locus genome-wide association mapping methods were used to quantify standing genetic variation for insecticide resistance in these populations and to identify specific alleles associated with insecticide survival. For each insecticide treatment, we estimated the proportion of the variation in survival explained by the genetic data (i.e. 'chip' heritability) and the number and contribution of individual loci with measurable effects. For all treatments, survival to an insecticide exposure was heritable with a polygenic architecture. Both P. papatasi and L. longipalpis had alleles for survival that resided within many genes throughout their genomes. The implications for resistance conferred by many alleles, as well as inferences made about the utility of laboratory insecticide resistance association studies compared to field observations, are discussed in the manuscript that accompanies this data.

opencc-zeroDec 2015View details →

Data from: Population scale mapping of transposable element diversity reveals links to gene regulation and epigenomic variation

Variation in the presence or absence of transposable elements (TEs) is a major source of genetic variation between individuals. Here, we identified 23,095 TE presence/absence variants between 216 Arabidopsis accessions. Most TE variants were rare, and we find these rare variants associated with local extremes of gene expression and DNA methylation levels within the population. Of the common alleles identified, two thirds were not in linkage disequilibrium with nearby SNPs, implicating these variants as a source of novel genetic diversity. Many common TE variants were associated with significantly altered expression of nearby genes, and a major fraction of inter-accession DNA methylation differences were associated with nearby TE insertions. Overall, this demonstrates that TE variants are a rich source of genetic diversity that likely plays an important role in facilitating epigenomic and transcriptional differences between individuals, and indicates a strong genetic basis for epigenetic variation.

Data from: Selection for population specific adaptation has shaped patterns of variation in the photoperiod pathway genes in Arabidopsis lyrata during post glacial colonization

Spatially varying selection can lead to population-specific adaptation, which is often recognized at the phenotypic level; however, the genetic evidence is weaker in many groups of organisms. In plants, environmental shifts that occur due to colonization of a novel environment may require adaptive changes in the timing of growth and flowering, which are often governed by location-specific environmental cues such as day length. We studied locally varying selection in 19 flowering time loci in nine populations of the perennial herb Arabidopsis lyrata, which has a wide but patchy distribution in temperate and boreal regions of the northern hemisphere. The populations differ in their recent population demographic and colonization histories and current environmental conditions, especially in the growing season length. We searched for population-specific molecular signatures of directional selection by comparing a set of candidate flowering time loci with a genomic reference set within each population using multiple approaches and contrasted the patterns of different populations. The candidate loci possessed approximately 20 % of the diversity of the reference loci. On average the flowering time loci had more rare alleles (a smaller Tajima's D) and an excess of highly differentiated sites relative to the reference, suggesting positive selection. The strongest signal of selection was detected in photoperiodic pathway loci in the colonizing populations of Northwestern Europe, whereas no evidence of positive selection was detected in the Central European populations. These findings emphasized the population-specific nature of selection and suggested that photoperiodic adaptation was important during post-glacial colonization of the species.

opencc-zeroDec 2013View details →

Data from: Intraspecific phenotypic variation among alewife populations drives parallel phenotypic shifts in bluegill

Evolutionary diversification within consumer species may generate selection on local ecological communities, affecting prey community structure. However, the extent to which this niche construction can propagate across food webs and shape trait variation in competing species is unknown. Here, we tested whether niche construction by different life-history variants of the planktivorous fish alewife (Alosa pseudoharengus) can drive phenotypic divergence and resource use in the competing species bluegill (Lepomis macrochirus). Using a combination of common garden experiments and a comparative field study, we found that bluegill from landlocked alewife lakes grew relatively better when fed small than large zooplankton, had gill rakers better adapted for feeding on small-bodied prey and selected smaller zooplankton compared with bluegill from lakes with anadromous or no alewife. Observed shifts in bluegill foraging traits in lakes with landlocked alewife parallel those in alewife, suggesting interspecific competition leading to parallel phenotypic changes rather than to divergence (which is commonly predicted). Our findings suggest that species may be locally adapted to prey communities structured by different life-history variants of a competing dominant species.

Data from: Genetic diversity does not explain variation in extra-pair paternity in multiple populations of a songbird

Many songbirds are socially monogamous but genetically polyandrous, mating with individuals outside their pair bonds. Extra-pair paternity (EPP) varies within and across species, but reasons for this variation remain unclear. One possible source of variation is population genetic diversity, which has been shown in interspecific meta-analyses to correlate with EPP but which has limited support from intraspecific tests. Using eight populations of the genetically polyandrous red-winged blackbird (Agelaius phoeniceus), including an island population, we investigated whether population-level differences in genetic diversity led to differences in EPP. We first measured genetic diversity over ten microsatellite loci and found, as predicted, low genetic diversity in the island population. Additional structure analyses with multilocus genotypes and mtDNA showed the island population to be distinct from the continental populations. However, the island population's EPP rate fell in the middle of the continental populations' distribution, while the continental populations themselves showed significant variation in EPP. This result suggests that genetic diversity by itself is not a predictor of EPP rate. We discuss reasons for the departure from previous results, including hypotheses for EPP that do not solely implicate female-driven behavior.

Data from: Comparing G: multivariate analysis of genetic variation in multiple populations

The additive genetic variance–covariance matrix (G) summarizes the multivariate genetic relationships among a set of traits. The geometry of G describes the distribution of multivariate genetic variance, and generates genetic constraints that bias the direction of evolution. Determining if and how the multivariate genetic variance evolves has been limited by a number of analytical challenges in comparing G-matrices. Current methods for the comparison of G typically share several drawbacks: metrics that lack a direct relationship to evolutionary theory, the inability to be applied in conjunction with complex experimental designs, difficulties with determining statistical confidence in inferred differences and an inherently pair-wise focus. Here, we present a cohesive and general analytical framework for the comparative analysis of G that addresses these issues, and that incorporates and extends current methods with a strong geometrical basis. We describe the application of random skewers, common subspace analysis, the 4th-order genetic covariance tensor and the decomposition of the multivariate breeders equation, all within a Bayesian framework. We illustrate these methods using data from an artificial selection experiment on eight traits in Drosophila serrata, where a multi-generational pedigree was available to estimate G in each of six populations. One method, the tensor, elegantly captures all of the variation in genetic variance among populations, and allows the identification of the trait combinations that differ most in genetic variance. The tensor approach is likely to be the most generally applicable method to the comparison of G-matrices from any sampling or experimental design.

Data from: Variation in costs of parasite resistance among natural host populations

Organisms that can resist parasitic infection often have lower fitness in the absence of parasites. These costs of resistance can mediate host evolution during parasite epidemics. For example, large epidemics will select for increased host resistance. In contrast, small epidemics (or no disease) can select for increased host susceptibility when costly resistance allows more susceptible hosts to outcompete their resistant counterparts. Despite their importance for evolution in host populations, costs of resistance (which are also known as resistance trade-offs) have mainly been examined in laboratory-based host-parasite systems. Very few examples come from field-collected hosts. Furthermore, little is known about how resistance trade-offs vary across natural populations. We addressed these gaps using the freshwater crustacean Daphnia dentifera and its natural yeast parasite, Metschnikowia bicuspidata. We found a cost of resistance in two of the five populations we studied – those with the most genetic variation in resistance and the smallest epidemics in the previous year. However, yeast epidemics in the current year did not alter slopes of these trade-offs before and after epidemics. In contrast, the no-cost populations showed little variation in resistance, possibly because large yeast epidemics eroded that variation in the previous year. Consequently, our results demonstrate variation in costs of resistance in wild host populations. This variation has important implications for host evolution during epidemics in nature.

opencc-zeroDec 2013View details →

Data from: Combining animal personalities with transcriptomics resolves individual variation within a wild-type zebrafish population and identifies underpinning molecular differences in brain function

Resolving phenotype variation within a population in response to environmental perturbation is central to understanding biological adaptation. Relating meaningful adaptive changes at the level of the transcriptome requires the identification of processes that have a functional significance for the individual. This remains a major objective towards understanding the complex interactions between environmental demand and an individual's capacity to respond to such demands. The interpretation of such interactions and the significance of biological variation between individuals from the same or different populations remain a difficult and under-addressed question. Here, we provide evidence that variation in gene expression between individuals in a zebrafish population can be partially resolved by a priori screening for animal personality and accounts for >9% of observed variation in the brain transcriptome. Proactive and reactive individuals within a wild-type population exhibit consistent behavioural responses over time and context that relates to underlying differences in regulated gene networks and predicted protein–protein interactions. These differences can be mapped to distinct regions of the brain and provide a foundation towards understanding the coordination of underpinning adaptive molecular events within populations.

Data from: Population size is weakly related to quantitative genetic variation and trait differentiation in a stream fish

How population size influences quantitative genetic variation and differentiation among natural, fragmented populations remains unresolved. Small, isolated populations might occupy poor quality habitats and lose genetic variation more rapidly due to genetic drift than large populations. Genetic drift might furthermore overcome selection as population size decreases. Collectively, this might result in directional changes in additive genetic variation (VA) and trait differentiation (QST) from small to large population size. Alternatively, small populations might exhibit larger variation in VA and QST if habitat fragmentation increases variability in habitat types. We explored these alternatives by investigating VA and QST using nine fragmented populations of brook trout varying 50-fold in census size N (179-8416) and 10-fold in effective number of breeders, Nb (18-135). Across 15 traits, no evidence was found for consistent differences in VA and QST with population size and almost no evidence for increased variability of VA or QST estimates at small population size. This suggests that (i) small populations of some species may retain adaptive potential according to commonly adopted quantitative genetic measures and (ii) populations of varying sizes experience a variety of environmental conditions in nature, however extremely large studies are likely required before any firm conclusions can be made.

Data from: Variation in thermal performance and reaction norms among populations of Drosophila melanogaster

The major goal of evolutionary thermal biology is to understand how variation in temperature shapes phenotypic evolution. Comparing thermal reaction norms among populations from different thermal environments allows us to gain insights into the evolutionary mechanisms underlying thermal adaptation. Here, we have examined thermal adaptation in six wild populations of the fruit fly (Drosophila melanogaster) from markedly different natural environments by analyzing thermal reaction norms for fecundity, thorax length, wing area and ovariole number under ecologically realistic fluctuating temperature regimes in the laboratory. Contrary to expectation, we found only minor differences in the thermal optima for fecundity among populations. Differentiation among populations was mainly due to differences in absolute (and partly also relative) thermal fecundity performance. Despite significant variation among populations in the absolute values of morphological traits, we observed only minor differentiation in their reaction norms. Overall, the thermal reaction norms for all traits examined were remarkably similar among different populations. Our results therefore suggest that thermal adaptation in D. melanogaster predominantly involves evolutionary changes in absolute trait values rather than in aspects of thermal reaction norms.

opencc-zeroDec 2009View details →

Data from: Low demographic variability in wild primate populations: fitness impacts of variation, covariation, and serial correlation in vital rates

In a stochastic environment, long-term fitness can be influenced by variation, covariation, and serial correlation in vital rates (survival and fertility). Yet no study of an animal population has parsed the contributions of these three aspects of variability to long-term fitness. We do so using a unique database that includes complete life history information for wild-living individuals of seven primate species that have been the subjects of long-term (22 to 45 year) behavioral studies. Overall, the estimated levels of vital rate variation had only minor effects on long-term fitness, and the effects of vital rate covariation and serial correlation were even weaker. To explore why, we compared estimated variances of adult survival in primates to values for other vertebrates in the literature, and found that adult survival is significantly less variable in primates than in the other vertebrates. Finally, we tested the prediction that adult survival, because it more strongly influences fitness in a constant environment, will be less variable than newborn survival, and found only mixed support for the prediction. Our results suggest that wild primates may be buffered against detrimental fitness effects of environmental stochasticity by their highly developed cognitive abilities, social networks, and broad, flexible diets.

opencc-zeroDec 2015View details →

Data from: Influence of introduction history on genetic variation in introduced populations: a case study of Oregon Chub

Population introductions and reintroductions have become a common tool for conserving threatened species, but oftentimes introduced populations have reduced the genetic diversity compared with the source population they were founded from. Population introductions played an important role in the recovery of the Oregon Chub Oregonichthys crameri, a small floodplain minnow found in western Oregon. Unlike many introduction efforts, introduced populations of Oregon Chub were founded using large numbers of individuals (hundreds in many cases) and each population had a unique introduction history (e.g., number of founders, source populations selected, duration of the introduction effort). We used microsatellite loci to examine 13 introduced populations and their respective sources to evaluate how well the introduction program captured genetic diversity present in the wild populations. Genetic variation was reduced by roughly 25% in one introduced population, and three introduced populations showed evidence of a genetic bottleneck due to heterozygote excess. Populations introduced from multiple sources had greater genetic diversity than populations from a single source. When multiple source populations were used, all source populations contributed genetic material to the introduced population, though the proportional contribution from each source population varied. Using correlation analyses and general linear models, we explored the relationship between introduction history variables and genetic diversity. Our top-ranked models included genetic diversity in the source population, and this variable had the highest variable importance weight (0.999), but the number of founders and the number of source populations were also important. Overall, the Oregon Chub introduction program was highly successful at capturing the genetic variation observed in natural populations. Results of this study will be useful for planning future population introductions for Oregon Chub and other species of conservation concern.

Data from: Temporal variation favors the evolution of generalists in experimental populations of Drosophila melanogaster

In variable environments, selection should favor generalists that maintain fitness across a range of conditions. However, costs of adaptation may generate fitness trade-offs and lead to some compromise between specialization and generalization that maximizes fitness. Here, we evaluate the evolution of specialization and generalization in 20 populations of Drosophila melanogaster experimentally evolved in constant and variable thermal environments for 3 years. We developed genotypes from each population at two temperatures after which we measured fecundity across eight temperatures. We predicted that constant environments would select for thermal specialists and that variable environments would select for thermal generalists. Contrary to our predictions, specialists and generalists did not evolve in constant and spatially variable environments, respectively. However, temporal variation produced a type of generalist that has rarely been considered by theoretical models of developmental plasticity. Specifically, genotypes from the temporally variable selective environment were more fecund across all temperatures than were genotypes from other environments. These patterns suggest certain allelic effects and should inspire new directions for modeling adaptation to fluctuating environments.

opencc-zeroDec 2017View details →

Data from: Individual variation, population-specific behaviours, and stochastic processes shape marine migration phenologies

1. The phenology of long distance migrations can influence individual fitness, moderate population dynamics, and regulate the availability of ecosystem services to other trophic levels. Phenology varies within and among populations, and can be influenced by conditions individuals experience both prior to departure and encounter en route. 2. Assessing how intrinsic and extrinsic factors (e.g. individual physical condition vs. environmental conditions) interact to influence variation in migratory phenologies across ecological scales is often limited due to logistical constraints associated with tracking large numbers of individuals from multiple populations simultaneously. 3. We used two natural tags, DNA and otolith microstructure analysis, to estimate the relative influence of individual traits (life history strategy, body size at departure, and growth during migration), population-specific strategies, and interannual variability on the phenology of marine migrations in juvenile sockeye salmon Oncorhynchus nerka. 4. We show that the timing and duration of juvenile sockeye salmon migrations were correlated with both life history strategy and body size, while migration duration was also correlated with departure timing and growth rates during migration. Even after accounting for the effect of individual traits, several populations exhibited distinct migration phenologies. Finally, we observed substantial interannual and residual variation, suggesting stochastic environmental conditions moderate the influence of carry-over effects that develop prior to departure, as well as population-specific strategies. 5. Migratory phenologies are shaped by complex interactions between drivers acting at multiple ecological and temporal scales. Given evidence that intraspecific diversity can stabilize ecological systems, conservation efforts should seek to maintain migratory variation among populations and preserve locally adapted phenotypes; however, variation within populations, which may buffer systems from environmental stochasticity, should also be regularly assessed and preserved.

opencc-zeroDec 2016View details →

Data from: Population genomic analysis suggests strong influence of river network on spatial distribution of genetic variation in invasive saltcedar across the southwestern US

Understanding the complex influences of landscape and anthropogenic elements that shape the population genetic structure of invasive species provides insight into patterns of colonization and spread. The application of landscape genomics techniques to these questions may offer detailed, previously undocumented insights into factors influencing species invasions. We investigated the spatial pattern of genetic variation and the influences of landscape factors on population similarity in the invasive riparian shrub saltcedar (Tamarix L.) by analyzing 1,997 genome-wide SNP markers for 259 individuals from 25 populations collected throughout the southwestern US. Our results revealed a broad-scale spatial genetic differentiation of saltcedar populations between the Colorado and Rio Grande river basins and identified potential barriers to population similarity along both river systems. River pathways most strongly contributed to population similarity. In contrast, low temperature and dams likely served as barriers to population similarity. We hypothesize that large-scale geographic patterns in genetic diversity resulted from a combination of early introductions from distinct populations, the subsequent influence of natural selection, dispersal barriers, and founder effects during range expansion.

opencc-zeroDec 2015View details →

Data from: Conserved genetic architecture underlying recombination rate variation in a wild population of Soay sheep (Ovis aries)

Meiotic recombination breaks down linkage disequilibrium and forms new haplotypes, meaning that it is an important driver of diversity in eukaryotic genomes. Understanding the causes of variation in recombination rate is important in interpreting and predicting evolutionary phenomena and for understanding the potential of a population to respond to selection. However, despite attention in model systems, there remains little data on how recombination rate varies at the individual level in natural populations. Here, we used extensive pedigree and high-density SNP information in a wild population of Soay sheep (Ovis aries) to investigate the genetic architecture of individual autosomal recombination rate. Individual rates were high relative to other mammal systems, and were higher in males than in females (autosomal map lengths of 3748 cM and 2860 cM, respectively). The heritability of autosomal recombination rate was low but significant in both sexes (h2 = 0.16 & 0.12 in females and males, respectively). In females, 46.7% of the heritable variation was explained by a sub-telomeric region on chromosome 6; a genome-wide association study showed the strongest associations at the locus RNF212, with further associations observed at a nearby ~374kb region of complete linkage disequilibrium containing three additional candidate loci, CPLX1, GAK and PCGF3. A second region on chromosome 7 containing REC8 and RNF212B explained 26.2% of the heritable variation in recombination rate in both sexes. Comparative analyses with 40 other sheep breeds showed that haplotypes associated with recombination rates are both old and globally distributed. Both regions have been implicated in rate variation in mice, cattle and humans, suggesting a common genetic architecture of recombination rate variation in mammals.

opencc-zeroDec 2013View details →

Data from: Density-mediated carry-over effects explain variation in breeding output across time in a seasonal population

In seasonal environments, where density dependence can operate throughout the annual cycle, vital rates are typically considered to be a function of the number of individuals at the beginning of each season. However, variation in density in the previous season could also cause surviving individuals to be in poor physiological condition, which could carry over to influence individual success in the following season. We examine this hypothesis using replicated populations of Drosophila melanogaster, the common fruitfly, over 23 non-overlapping generations with distinct breeding and non-breeding seasons. We found that the density at the beginning of the non-breeding season negatively affected the fresh weight of individuals that survived the non-breeding season and resulted in a 25% decrease in per capita breeding output among those that survived to the next season to breed. At the population level, per capita breeding output was best explained by a model that incorporated density at the beginning of the previous non-breeding season (carry-over effect, COE) and density at the beginning of the breeding season. Our results support the idea that density-mediated COEs are critical for understanding population dynamics in seasonal environments.

Data from: Spatially variable habitat quality contributes to within-population variation in reproductive success

Variation in habitat quality is common across terrestrial, freshwater, and marine habitats. We investigated how habitat quality influenced the reproductive potential of mud crabs across 30 oyster reefs that were degraded to different extents. We further coupled this field survey with a laboratory experiment designed to mechanistically determine the relationship between resource consumption and reproductive performance. We show a >10-fold difference in average reproductive potential for crabs across reefs of different quality. Calculated consumption rates for crabs in each reef, based on a type II functional response, suggest that differences in reproductive performance may be attributed to resource limitation in poor quality reefs. This conclusion is supported by results of our laboratory experiment where crabs fed a higher quality diet of abundant animal tissue had greater reproductive performance. Our results demonstrate that spatial variation in habitat quality can be a considerable contributor to within-population individual variation in reproductive success (i.e., demographic heterogeneity). This finding has important implications for assessing population extinction risk.