Evolution In Natural Populations Research Articles

A power–efficiency trade‐off in resource use alters epidemiological relationships

Trade-offs play pivotal roles in the ecology and evolution of natural populations. However, trade-offs are probably not static, invariant relationships. Instead, ecological factors can shift, alter, or reverse the relationships underlying trade-offs and create critical genotype x environment (G x E) interactions. But which ecological factors alter trade-offs or create G x E interactions, and why (mechanistically) do they do this? We tackle these questions using resource quality as the central ecological factor and a case study of disease in the plankton. We show that clonal genotypes of a zooplankton host (Daphnia dentifera) exhibit a "power-efficiency" trade-off in resource use, where powerful (fast-feeding) host clones perform well on richer algal resources, but more efficient (slow-feeding) clones perform relatively well on poorer resources. This resource-based trade-off then influences epidemiological relationships due to fundamental connections between resources and fecundity, transmission rate (an index of resistance), and replication of a virulent fungal parasite (Metschnikowia bicuspidata) within hosts. For instance, using experiments and dynamic energy budget models, we show that the power-efficiency trade-off overturned a previously detected trade-off between fecundity and transmission risk of hosts to this parasite. When poorer resources were eaten, transmission risk and fecundity were negatively, not positively, correlated. Additionally, poor resource quality changed positive relationships between yield of infectious stages (spores) and host fecundity: those fecundity-spore relationships with poor food became negative or nonsignificant. Finally, the power-efficiency trade-off set up an interaction between host clone and resource quality for yield of fungal spores: powerful clones yielded relatively more spores on the better resource, while efficient clones yielded relatively more on the poorer resource. Thus, the physiological ecology of resource use can offer potent, mechanistic insight linking environmental factors to epidemiological relationships.

Spatio-Temporal Evolutionary Dynamics in Natural Butterfly Populations (2012 Field Season)

The study of evolution in natural populations has advanced our understanding of the origin and maintenance of biological diversity. For example, long term studies of wild populations indicate that natural selection can cause rapid and dramatic changes in traits, but that in some cases these evolutionary changes are quickly reversed when periodic variation in weather patterns or the biotic environment cause the optimal trait value to change (e.g., Reznick et al. 1997; Grant and Grant 2002). In fact, spatial and temporal variation in the strength and nature of natural selection could explain the high levels of genetic variation found in many natural populations (Gillespie 1994; Siepielski et al. 2009). Long term studies of evolution in the wild could also be informative for biodiversity conservation and resource management, because, for example, data on short term evolutionary responses to annual fluctuations in temperature or rainfall could be used to predict longer term evolution in response to directional climate change. Most previous research on evolution in the wild has considered one or a few observable traits or genes (Kapan 2001; Grant and Grant 2002; Barrett et al. 2008). We believe that more general conclusions regarding the rate and causes of evolutionary change in the wild and selection’s contribution to the maintenance of genetic variation could be obtained by studying genome-wide molecular evolution in a suite of natural populations. Thus, we have begun a long term study of genome-wide molecular evolution in a series of natural butterfly populations in the Greater Yellowstone Area (GYA). This study will allow us to quantify the contribution of environment-dependent natural selection to evolution in these butterfly populations and determine whether selection consistently favors the same alleles across space and through time.

A Genome-wide SNP Genotyping Array Reveals Patterns of Global and Repeated Species-Pair Divergence in Sticklebacks

Genes underlying repeated adaptive evolution in natural populations are still largely unknown. Stickleback fish (Gasterosteus aculeatus) have undergone a recent dramatic evolutionary radiation, generating numerous examples of marine-freshwater species pairs and a small number of benthic-limnetic species pairs found within single lakes [1]. We have developed a new genome-wide SNP genotyping array to study patterns of genetic variation in sticklebacks over a wide geographic range, and to scan the genome for regions that contribute to repeated evolution of marine-freshwater or benthic-limnetic species pairs. Surveying 34 global populations with 1,159 informative markers revealed substantial genetic variation, with predominant patterns reflecting demographic history and geographic structure. After correcting for geographic structure and filtering for neutral markers, we detected large repeated shifts in allele frequency at some loci, identifying both known and novel loci likely contributing to marine-freshwater and benthic-limnetic divergence. Several novel loci fall close to genes implicated in epithelial barrier or immune functions, which have likely changed as sticklebacks adapt to contrasting environments. Specific alleles differentiating sympatric benthic-limnetic species pairs are shared in nearby solitary populations, suggesting an allopatric origin for adaptive variants and selection pressures unrelated to sympatry in the initial formation of these classic vertebrate species pairs.

Recombination rate variation in closely related species.

Despite their importance to successful meiosis and various evolutionary processes, meiotic recombination rates sometimes vary within species or between closely related species. For example, humans and chimpanzees share virtually no recombination hotspot locations in the surveyed portion of the genomes. However, conservation of recombination rates between closely related species has also been documented, raising an apparent contradiction. Here, we evaluate how and why conflicting patterns of recombination rate conservation and divergence may be observed, with particular emphasis on features that affect recombination, and the scale and method with which recombination is surveyed. Additionally, we review recent studies identifying features influencing fine-scale and broad-scale recombination patterns and informing how quickly recombination rates evolve, how changes in recombination impact selection and evolution in natural populations, and more broadly, which forces influence genome evolution.

EXPLORING POSSIBLE HUMAN INFLUENCES ON THE EVOLUTION OF DARWIN'S FINCHES

Humans are an increasingly common influence on the evolution of natural populations. Potential arenas of influence include altered evolutionary trajectories within populations and modifications of the process of divergence among populations. We consider this second arena in the medium ground finch (Geospiza fortis) on Santa Cruz Island, Galápagos, Ecuador. Our study compared the G. fortis population at a relatively undisturbed site, El Garrapatero, to the population at a severely disturbed site, Academy Bay, which is immediately adjacent to the town of Puerto Ayora. The El Garrapatero population currently shows beak size bimodality that is tied to assortative mating and disruptive selection, whereas the Academy Bay population was historically bimodal but has lost this property in conjunction with a dramatic increase in local human population density. We here evaluate potential ecological-adaptive drivers of the differences in modality by quantifying relationships between morphology (beak and head dimensions), functional performance (bite force), and environmental characteristics (diet). Our main finding is that associations among these variables are generally weaker at Academy Bay than at El Garrapatero, possibly because novel foods are used at the former site irrespective of individual morphology and performance. These results are consistent with the hypothesis that the rugged adaptive landscapes promoting and maintaining diversification in nature can be smoothed by human activities, thus hindering ongoing adaptive radiation.

Epistasis and environmental heterogeneity in the speciation process

The study of evolutionary mechanisms driving evolution of natural populations is a central issue in evolutionary biology. In this context the question of genetic divergence and speciation in ecosystems is one of the most intriguing and complex challenges nowadays. The current manuscript aims to investigate the aforementioned problem by means of extensive computer simulations. Here we introduce a spatial model of evolution which assumes viability selection, mutations and random mating. The population evolves in a heterogeneous environment where the habitat diversity is an input of the model. As a model for the fitness landscape a variation of the NK model is assumed. We present results for the time evolution of fitness and genetic divergence and address the species-area relationship. The dependence of the quantities and scalings of the problem with epistasis is investigated. Depending on the mutation rate, the species-area relationship displays either two-phase or a triphasic scenario. In any case, for intermediate and large system sizes the relationship is well described by a power-law, with exponents within the range of values observed in real ecological niches. All the quantities show a strong dependence on the epistasis parameter. According to our simulations, a lower level of genetic divergence is needed in order to ensure sexual isolation when interactions among genes is strong.

Morphological response of songbirds to 100 years of landscape change in North America

Major landscape changes caused by humans may create strong selection pressures and induce rapid evolution in natural populations. In the last 100 years, eastern North America has experienced extensive clear-cutting in boreal areas, while afforestation has occurred in most temperate areas. Based on museum specimens, I show that wings of several boreal forest songbirds and temperate songbirds of non-forest habitats have become more pointed over the last 100 years. In contrast, wings of most temperate forest and early-successional boreal forests species have become less pointed over the same period. In contrast to wing shape, the bill length of most species did not change significantly through time. These results are consistent with the "habitat isolation hypothesis", i.e., songbirds evolved in response to recent changes in the amount of available habitat and associated implications for mobility. Rapid morphological evolution may mitigate, without necessarily preventing, negative consequences of habitat loss caused by humans through direct exploitation or climate change.

Experimental alteration of DNA methylation affects the phenotypic plasticity of ecologically relevant traits in Arabidopsis thaliana

Heritable phenotypic variation in plants can be caused not only by underlying genetic differences, but also by variation in epigenetic modifications such as DNA methylation. However, we still know very little about how relevant such epigenetic variation is to the ecology and evolution of natural populations. We conducted a greenhouse experiment in which we treated a set of natural genotypes of Arabidopsis thaliana with the demethylating agent 5-azacytidine and examined the consequences of this treatment for plant traits and their phenotypic plasticity. Experimental demethylation strongly reduced the growth and fitness of plants and delayed their flowering, but the degree of this response varied significantly among genotypes. Differences in genotypes’ responses to demethylation were only weakly related to their genetic relatedness, which is consistent with the idea that natural epigenetic variation is independent of genetic variation. Demethylation also altered patterns of phenotypic plasticity, as well as the amount of phenotypic variation observed among plant individuals and genotype means. We have demonstrated that epigenetic variation can have a dramatic impact on ecologically important plant traits and their variability, as well as on the fitness of plants and their ecological interactions. Epigenetic variation may thus be an overlooked factor in the evolutionary ecology of plant populations.

Physiology and Global Climate Change

The analysis of how physiology affects the distribution and abundance of animals in nature has advanced along with the rest of physiology, finding its origins in the Law of the Minimum (1) and the Law of Tolerance (2). Two seminal advances were the reframing of these laws in terms of not just survival but the capacity of animals to be active (3) and recognizing the need to extend the study of the relevant physiology outside of the laboratory and into free-ranging organisms in nature (4). These advances in turn led to the explicit incorporation of principles of mass and energy exchange between organisms and their environment in nature [since termed biophysical ecology (5)] and of population and evolutionary biology [now termed evolutionary physiology (6, 7)]. Physiological analysis of animal distribution and abundance continues to reinvent itself with the incorporation of molecular, genomic, and systems approaches (8) and now finds a new role as it elucidates the consequences of rapid climate change. These efforts synergize with a growing recognition that rapid evolution in natural populations can occur on ecological timescales and hence affect ecological interactions and community dynamics (9).

Why is adaptation prevented at ecological margins? New insights from individual‐based simulations

All species are restricted in their distribution. Currently, ecological models can only explain such limits if patches vary in quality, leading to asymmetrical dispersal, or if genetic variation is too low at the margins for adaptation. However, population genetic models suggest that the increase in genetic variance resulting from dispersal should allow adaptation to almost any ecological gradient. Clearly therefore, these models miss something that prevents evolution in natural populations. We developed an individual-based simulation to explore stochastic effects in these models. At high carrying capacities, our simulations largely agree with deterministic predictions. However, when carrying capacity is low, the population fails to establish for a wide range of parameter values where adaptation was expected from previous models. Stochastic or transient effects appear critical around the boundaries in parameter space between simulation behaviours. Dispersal, gradient steepness, and population density emerge as key factors determining adaptation on an ecological gradient.

Eco‐genetic modeling of contemporary life‐history evolution

We present eco-genetic modeling as a flexible tool for exploring the course and rates of multi-trait life-history evolution in natural populations. We build on existing modeling approaches by combining features that facilitate studying the ecological and evolutionary dynamics of realistically structured populations. In particular, the joint consideration of age and size structure enables the analysis of phenotypically plastic populations with more than a single growth trajectory, and ecological feedback is readily included in the form of density dependence and frequency dependence. Stochasticity and life-history trade-offs can also be implemented. Critically, eco-genetic models permit the incorporation of salient genetic detail such as a population's genetic variances and covariances and the corresponding heritabilities, as well as the probabilistic inheritance and phenotypic expression of quantitative traits. These inclusions are crucial for predicting rates of evolutionary change on both contemporary and longer timescales. An eco-genetic model can be tightly coupled with empirical data and therefore may have considerable practical relevance, in terms of generating testable predictions and evaluating alternative management measures. To illustrate the utility of these models, we present as an example an eco-genetic model used to study harvest-induced evolution of multiple traits in Atlantic cod. The predictions of our model (most notably that harvesting induces a genetic reduction in age and size at maturation, an increase or decrease in growth capacity depending on the minimum-length limit, and an increase in reproductive investment) are corroborated by patterns observed in wild populations. The predicted genetic changes occur together with plastic changes that could phenotypically mask the former. Importantly, our analysis predicts that evolutionary changes show little signs of reversal following a harvest moratorium. This illustrates how predictions offered by eco-genetic models can enable and guide evolutionarily sustainable resource management.

Community monopolization: local adaptation enhances priority effects in an evolving metacommunity

The diversity and composition of biological communities might often depend on colonization history because early colonists can exclude future colonists through a priority effect. These priority effects, which have been observed across a wide variety of ecosystems, often arise because early colonists have sufficient time to use available resources efficiently and subsequently withhold them from invaders. Here, we explore the extent to which rapid local adaptive evolution contributes to the pervasiveness of these priority effects. Using an individual-based simulation, we show that early colonization allows the descendants of colonists to adapt to novel conditions and reduce the establishment success of an initially ecologically equivalent competing species. Our model predicts that slight differences in colonization timing and adaptive capacity between species can substantially alter the dynamics and diversity of communities. We also show that priority effects and gene flow can generate a novel mechanism for the expansion and retraction of species distributions in a metacommunity. Our results suggest that local adaptation combined with stochastic colonization events can obscure direct relationships between species distributions and environmental gradients. Given the increasing recognition of rapid, microgeographic evolution in natural populations, we expect that evolutionary priority effects could affect the structure and dynamics of many natural metacommunities.

Population genomics of marine fishes: identifying adaptive variation in space and time

Studies of adaptive evolution have experienced a recent revival in population genetics of natural populations and there is currently much focus on identifying genomic signatures of selection in space and time. Insights into local adaptation, adaptive response to global change and evolutionary consequences of selective harvesting can be generated through population genomics studies, allowing the separation of the effects invoked by neutral processes (drift-migration) from those due to selection. Such knowledge is important not only for improving our basic understanding of natural as well as human-induced evolutionary processes, but also for predicting future trajectories of biodiversity and for setting conservation priorities. Marine fishes possess a number of features rendering them well suited for providing general insights into adaptive genomic evolution in natural populations. These include well-described population structures, substantial and rapidly developing genomic resources and abundant archived samples enabling temporal studies. Furthermore, superior possibilities for conducting large-scale experiments under controlled conditions, due to the economic resources provided by the large and growing aquaculture industry, hold great promise for utilizing recent technological developments. Here, we review achievements in marine fish genomics to date and highlight potential avenues for future research, which will provide both general insights into evolution in high gene flow species, as well as specific knowledge which can lead to improved management of marine organisms.

NATURAL SELECTION REDUCES ENERGY METABOLISM IN THE GARDEN SNAIL,HELIX ASPERSA(CORNU ASPERSUM)

Phenotypic selection is widely recognized as the primary cause of adaptive evolution in natural populations, a fact that has been documented frequently over the last few decades, mainly in morphological and life-history traits. The energetic definition of fitness predicts that natural selection will maximize the residual energy available for growth and reproduction, suggesting that energy metabolism could be a target of selection. To address this problem, we chose the garden snail, Helix aspersa (Cornu aspersum). We performed a seminatural experiment for measuring phenotypic selection on standard metabolic rate (SMR), the minimum cost of maintenance in ectotherm organisms. To discount selection on correlated traits, we included two additional whole-organism performance traits (mean speed and maximum force of dislodgement). We found a combination of linear (negative directional selection, beta=-0.106 +/- 0.06; P= 0.001) and quadratic (stabilizing selection, gamma=-0.012 +/- 0.033; P= 0.061) selection on SMR. Correlational selection was not significant for any possible pair of traits. This suggests that individuals with average-to-reduced SMRs were promoted by selection. To the best of our knowledge, this is the first study showing significant directional selection on the obligatory cost of maintenance in an animal, providing support for the energetic definition of fitness.

Female preference for male body size in brown trout, Salmo trutta: is big still fashionable?

The study of female preference for male traits is of primary importance for understanding the role of sexual selection in the evolution of natural populations. Female preference is usually investigated in controlled conditions to facilitate the manipulation of variables. However, such results are rarely confirmed in wild populations where many variables act together. Inferring the role of female preference in the outcome of reproduction thus requires field studies and a specific approach to behavioural data. We observed, over 2 years, the courtship behaviours of male and female brown trout in six populations distributed along a French watershed. We focused on behavioural items linked to female preference for male body size. We built a behavioural model describing the relationships between behaviour and female preference and estimated the parameters of the model using a Bayesian modelling approach. We found a significant preference for body size ratio: females tended to prefer males at least 1.45 times their own size. This preference varied between populations and was influenced by female size. Operational sex ratio had only a weak influence on female preference. Our model explained 44% of the observed variation in behaviour. Finally, because observed body size ratio at mating was generally greater than 1, we conclude that female preference plays a major role in the outcome of reproduction in wild populations of brown trout. These results are compared with existing knowledge and theory and their possible consequences at the population level are discussed.

Synergistic, antagonistic and additive effects of multiple stressors: predation threat, parasitism and pesticide exposure in Daphnia magna

Summary Predation and parasitism are important factors in the ecology and evolution of natural populations and may, along with other environmental factors, interact with the impact of anthropogenic pollutants. Our study aimed at identifying potential interactions between three stressors (predation threat, parasitism and pesticide exposure) and at exploring the predictability of their joint effects by using the model of independent action. We assessed in a full‐factorial design the impacts of these stressors on key life‐history traits and population growth rate of the water flea Daphnia magna. When applied as single stressors, predation threat and parasite challenge induced varying stressor‐specific adaptive responses. The pesticide carbaryl was applied at a generally sublethal concentration, which caused low mortality only in first‐brood offspring. Pesticide exposure interacted synergistically with parasite challenge regarding survival, which suggests immunomodulatory activity of the pesticide. Predation threat by phantom midge larvae showed antagonistic interactions for amount of first‐brood offspring with both parasite challenge and carbaryl exposure. All stressors additively affected age and size at maturity, which added up to a considerable delay in the onset of reproduction in the three‐stressor combination. The intrinsic rate of natural increase, r, reflected the non‐additive and additive effects on single endpoints and showed significant synergistic interactions for all two‐stressor combinations. The combination of all stressors resulted in a dramatic reduction of r compared to the stressor‐free control. The model of independent action proved useful in quantitatively predicting effects of additively acting stressors, and in visualizing the occurrence and magnitude of non‐additive effects in accordance with results of analysis of variances. Synthesis and applications. Cumulative additive effects and non‐additive interactions of natural antagonists and pollutants are shown to result in considerable impacts on ecologically relevant parameters. As a starting point for an environmentally more realistic risk assessment of chemicals, it may be a valuable strategy to screen for non‐additive effects among many stress factors simultaneously in simplified experimental designs by using the model of independent action.

Relationships between morphological variance, gene diversity and flavonoid patterns in the land race populations of Ethiopian barley

Bekele, E. 1984. Relationships between morphological variance. gene diversity and flavonoid patterns in the land race populations of Ethiopian barley. —Hereditas 100: 271–294. Lund, Sweden. ISSN 0018–0661. Received February 7, 1984 An argument is forwarded that in addition to multiple genetic factors, single gene mutation with major effect could be very important in the evolution of natural populations and domesticates. The effect of null alleles and correlations between traits determined by major and minor genes are suggested to show different strategies of adaptation among different kinds of organisms. Sturtevant's hybrid dysgenesis could be the genetic reasons for Vavilov's emancipation of recessives. The three linked esterase loci are assumed to be the results of some form of gene duplication. The genetic backgrounds of the gene are reasons for unspecific polytype correlations between all states of genes and ecological variables. The rank correlation of the percentage of the contribution to the total variation by the differences between individuals in each population between enzymatic and morphological variation was not significant except for row number and Est-A locus. Diversity indices of morphological variables and enzymes are differently correlated in different regions. Enzyme variation and quantitative characters are positively correlated in some regions and negatively in others. But negative correlations are mainly concentrated into three regions. This, together with the result of kurtosis and skewness of quantitative characters are taken to be the results of multidirectional selection schemes. Correlations of quantitative characters showed an overall higher occurrence of negative correlations between plant height and number of sterile florets. Regional cluster differences based on genetic distance measures of enzymatic data and morphological data are perhaps due to differences in the fitness potential that can be related to particular allelic combinations at one level and more directly, to phenotypic properties at another. Enzyme variations and frequencies of flavonoid patterns are negatively correlated. The eleven frequent alleles that were correlated with means of six quantitative characters showed both negative and positive correlations with uneven distribution over regions. Flavonoid C pattern is negatively correlated with a number of sterile florets and positively correlated with a number of seeds.

A unified model for functional and statistical epistasis and its application in quantitative trait Loci analysis.

Interaction between genes, or epistasis, is found to be common and it is a key concept for understanding adaptation and evolution of natural populations, response to selection in breeding programs, and determination of complex disease. Currently, two independent classes of models are used to study epistasis. Statistical models focus on maintaining desired statistical properties for detection and estimation of genetic effects and for the decomposition of genetic variance using average effects of allele substitutions in populations as parameters. Functional models focus on the evolutionary consequences of the attributes of the genotype-phenotype map using natural effects of allele substitutions as parameters. Here we provide a new, general and unified model framework: the natural and orthogonal interactions (NOIA) model. NOIA implements tools for transforming genetic effects measured in one population to the ones of other populations (e.g., between two experimental designs for QTL) and parameters of statistical and functional epistasis into each other (thus enabling us to obtain functional estimates of QTL), as demonstrated numerically. We develop graphical interpretations of functional and statistical models as regressions of the genotypic values on the gene content, which illustrates the difference between the models--the constraint on the slope of the functional regression--and when the models are equivalent. Furthermore, we use our theoretical foundations to conceptually clarify functional and statistical epistasis, discuss the advantages of NOIA over previous theory, and stress the importance of linking functional and statistical models.

Genetic structure and evolution of natural populations of viruses causing the tomato yellow leaf curl disease in Spain

The population structure and genetic variation of two begomoviruses: tomato yellow leaf curl Sardinia virus (TYLCSV) and tomato yellow leaf curl virus (TYLCV) in tomato crops of Spain were studied from 1997 until 2001. Restriction digestion of a genomic region comprised of the CP coat protein gene (CPR) of 358 TYLC virus isolates enabled us to classify them into 14 haplotypes. Nucleotide sequences of two genomic regions: CPR, and the surrounding intergenic region (SIR) were determined for at least two isolates per haplotype. SIR was more variable than CPR and showed multiple recombination events whereas no recombination was detected within CPR. In all geographic regions except Murcia, the population was, or evolved to be composed of one predominant haplotype with a low genetic diversity (<0.0180). In Murcia, two successive changes of the predominant haplotype were observed in the best studied population. Phylogenetic analysis showed that the TYLCSV sequences determined clustered with sequences obtained from the GenBank of other TYLCSV Spanish isolates which were clearly separated from TYLCSV Italian isolates. Most of our TYLCV sequences were similar to those of isolates from Japan and Portugal, and the sequences obtained from TYLCV isolates from the Canary island of Lanzarote were similar to those of Caribbean TYLCV isolates.

Introduction. Antarctic ecology: from genes to ecosystems. Part 2. Evolution, diversity and functional ecology

The Antarctic biota has evolved over the last 100 million years in increasingly isolated and cold conditions. As a result, Antarctic species, from micro-organisms to vertebrates, have adapted to life at extremely low temperatures, including changes in the genome, physiology and ecological traits such as life history. Coupled with cycles of glaciation that have promoted speciation in the Antarctic, this has led to a unique biota in terms of biogeography, patterns of species distribution and endemism. Specialization in the Antarctic biota has led to trade-offs in many ecologically important functions and Antarctic species may have a limited capacity to adapt to present climate change. These include the direct effects of changes in environmental parameters and indirect effects of increased competition and predation resulting from altered life histories of Antarctic species and the impacts of invasive species. Ultimately, climate change may alter the responses of Antarctic ecosystems to harvesting from humans. The unique adaptations of Antarctic species mean that they provide unique models of molecular evolution in natural populations. The simplicity of Antarctic communities, especially from terrestrial systems, makes them ideal to investigate the ecological implications of climate change, which are difficult to identify in more complex systems.