A multivariate test of evolutionary constraints for thermal tolerance in Drosophila melanogaster

Exposure to extreme temperatures is increasingly likely to impose strong selection on many organisms in their natural environments. The ability of organisms to adapt to such selective pressures will be determined by patterns of genetic variation and covariation. Despite increasing interest in thermal adaptation, few studies have examined the extent to which the genetic covariance between traits might constrain thermal responses. Furthermore, it remains unknown whether sex‐specific genetic architectures will constrain responses to climatic selection. We used a paternal half‐sibling breeding design to examine whether sex‐specific genetic architectures and genetic covariances between traits might constrain evolutionary responses to warming climates in a population of Drosophila melanogaster. Our results suggest that the sexes share a common genetic underpinning for heat tolerance as indicated by a strong positive inter‐sexual genetic correlation. Further, we found no evidence in either of the sexes that genetic trade‐offs between heat tolerance and fitness will constrain responses to thermal selection. Our results suggest that neither trade‐offs, nor sex‐specific genetics, will significantly constrain an evolutionary response to climatic warming, at least in this population of D. melanogaster.     

Rethinking adaptation: the niche-construction perspective

Niche construction refers to the capacity of organisms to construct, modify, and select important components of their local environments, such as nests, burrows, pupal cases, chemicals, and nutrients. A small but increasing number of evolutionary biologists regard niche construction as an evolutionary process in its own right, rather than as a mere product of natural selection. Through niche construction organisms not only influence the nature of their world, but also in part determine the selection pressures to which they and their descendants are exposed, and they do so in a non-random manner. Mathematical population genetics analyses have revealed that niche construction is likely to be evolutionarily consequential because of the feedback that it generates in the evolutionary process. A parallel movement has emerged in ecosystem ecology, where researchers stress the utility of regarding organisms as ecosystem engineers, who partly control energy and matter flows. From the niche construction standpoint, the evolving complementary match between organisms and environments is the product of reciprocal interacting processes of natural selection and niche construction. This essay reviews the arguments put forward in favor of the niche-construction perspective.     

Expressed sequence tag-linked microsatellites as a source of gene-associated polymorphisms for detecting signatures of divergent selection in atlantic salmon (Salmo salar L.)

The prediction that selection affects the genome in a locus-specific way also affecting flanking neutral variation, known as genetic hitchhiking, enables the use of polymorphic markers in noncoding regions to detect the footprints of selection. However, as the strength of the selective footprint on a locus depends on the distance from the selected site and will decay with time due to recombination, the utilization of polymorphic markers closely linked to coding regions of the genome should increase the probability of detecting the footprints of selection as more gene-containing regions are covered. The occurrence of highly polymorphic microsatellites in the untranslated regions of expressed sequence tags (ESTs) is a potentially useful source of gene-associated polymorphisms which has thus far not been utilized for genome screens in natural populations. In this study, we searched for the genetic signatures of divergent selection by screening 95 genomic and EST-derived mini- and microsatellites in eight natural Atlantic salmon, Salmo salar L., populations from different spatial scales inhabiting contrasting natural environments (salt-, brackish, and freshwater habitat). Altogether, we identified nine EST-associated microsatellites, which exhibited highly significant deviations from the neutral expectations using different statistical methods at various spatial scales and showed similar trends in separate population samples from different environments (salt-, brackish, and freshwater habitats) and sea areas (Barents vs. White Sea). We consider these ESTs as the best candidate loci affected by divergent selection, and hence, they serve as promising genes associated with adaptive divergence in Atlantic salmon. Our results demonstrate that EST-linked microsatellite genome scans provide an efficient strategy for discovering functional polymorphisms, especially in nonmodel organisms.     

The evolutionary consequences of niche construction: a theoretical investigation using two-locus theory

This paper addresses the joint evolution of environment-altering (niche constructing) traits, and traits whose fitness depends on alterable sources of natural selection in environments. We explore the evolutionary consequences of this niche construction using a two-locus population genetic model. The novel conclusions are that niche construction can (1) cause evolutionary inertia and momentum, (2) lead to the fixation of otherwise deleterious alleles, (3) support stable polymorphisms where none are expected, (4) eliminate what would otherwise be stable polymorphisms, and (5) influence disequilibrium. The results suggest that the changes that organisms bring about in their niche can themselves be an important source of natural selection pressures, and imply that evolution may proceed in cycles of selection and niche construction.     

Human dental reduction: natural selection or the probable mutation effect

Dental reduction has been sufficiently widespread among human populations to render the phenomenon of reduced tooth size worthy of scientific explanation. One of the most controversial models invoked to explain structural reduction in organisms is referred to as the "probable mutation effect" (PME). According to this model, structures no longer functional owing to ecological or cultural changes will experience a relaxation of selection pressure, permitting an accumulation of mutations in the population that inevitably will result in the reduction in size or the loss of the concerned structure. Although the PME continues to be offered as a viable explanation of human dental reduction, it is based upon several premises that modern dental clinical experience fails to support. Known enzyme defects resulting from mutations, factors predisposing to dental infections, and the deleterious effects of teeth that are too large or too small reveal that the PME does not logically account for the reduction of tooth size. Given such information, this paper proposes models of dental reduction based upon natural selection, which, unlike the PME, are testable in both modern and archaeological populations. The integration of clinical and skeletal data permits a more thorough understanding of dental reduction in the hominid fossil record.     

Predicting population genetic change in an autocorrelated random environment: Insights from a large automated experiment

Most natural environments exhibit a substantial component of random variation, with a degree of temporal autocorrelation that defines the color of environmental noise. Such environmental fluctuations cause random fluctuations in natural selection, affecting the predictability of evolution. But despite long-standing theoretical interest in population genetics in stochastic environments, there is a dearth of empirical estimation of underlying parameters of this theory. More importantly, it is still an open question whether evolution in fluctuating environments can be predicted indirectly using simpler measures, which combine environmental time series with population estimates in constant environments. Here we address these questions by using an automated experimental evolution approach. We used a liquid-handling robot to expose over a hundred lines of the micro-alga Dunaliella salina to randomly fluctuating salinity over a continuous range, with controlled mean, variance, and autocorrelation. We then tracked the frequencies of two competing strains through amplicon sequencing of nuclear and choloroplastic barcode sequences. We show that the magnitude of environmental fluctuations (determined by their variance), but also their predictability (determined by their autocorrelation), had large impacts on the average selection coefficient. The variance in frequency change, which quantifies randomness in population genetics, was substantially higher in a fluctuating environment. The reaction norm of selection coefficients against constant salinity yielded accurate predictions for the mean selection coefficient in a fluctuating environment. This selection reaction norm was in turn well predicted by environmental tolerance curves, with population growth rate against salinity. However, both the selection reaction norm and tolerance curves underestimated the variance in selection caused by random environmental fluctuations. Overall, our results provide exceptional insights into the prospects for understanding and predicting genetic evolution in randomly fluctuating environments.     

论达尔文医学(Ⅱ)

一切生物功能的设计都用查理士·达尔文的自然选择理论来解释,是本文中贯彻始终的思想．探讨的中心是自然选择所挑选的适应性变化这一概念：我们与病原格斗适应性变化,病原对抗这变化而产生的适应性变化,我们为了这些变化必须付出代价而出现的不适应性,以及机体设计和现在的生活环境之间的不适应性,等等．我们希望读者将在对身体的功能以及某些异常情况的进化论解释中得到教益．     

Differentiation of reproductive and competitive ability in the invaded range of Senecio inaequidens: the role of genetic Allee effects, adaptive and nonadaptive evolution

Genetic differentiation in the competitive and reproductive ability of invading populations can result from genetic Allee effects or r/K selection at the local or range-wide scale. However, the neutral relatedness of populations may either mask or falsely suggest adaptation and genetic Allee effects. In a common-garden experiment, we investigated the competitive and reproductive ability of invasive Senecio inaequidens populations that vary in neutral genetic diversity, population age and field vegetation cover. To account for population relatedness, we analysed the experimental results with 'animal models' adopted from quantitative genetics. Consistent with adaptive r/K differentiation at local scales, we found that genotypes from low-competition environments invest more in reproduction and are more sensitive to competition. By contrast, apparent effects of large-scale r/K differentiation and apparent genetic Allee effects can largely be explained by neutral population relatedness. Invading populations should not be treated as homogeneous groups, as they may adapt quickly to small-scale environmental variation in the invaded range. Furthermore, neutral population differentiation may strongly influence invasion dynamics and should be accounted for in analyses of common-garden experiments.     

论达尔文医学(Ⅰ)

一切生物功能的设计都用查理士．达尔文的的自然选择理论来解释,是本文中贯彻始终的思想,探讨的中心自然自动所控制所挑选的适应性变化这一概念：我们与病原格斗适应性变化,病原对抗这变而产生的知识性变化。     

Niche construction and the environmental term of the price equation: How natural selection changes when organisms alter their environments

Organisms construct their own environments and phenotypes through the adaptive processes of habitat choice, habitat construction, and phenotypic plasticity. We examine how these processes affect the dynamics of mean fitness change through the environmental change term of the Price Equation. This tends to be ignored in evolutionary theory, owing to the emphasis on the first term describing the effect of natural selection on mean fitness (the additive genetic variance for fitness of Fisher's Fundamental Theorem). Using population genetic models and the Price Equation, we show how adaptive niche constructing traits favorably alter the distribution of environments that organisms encounter and thereby increase population mean fitness. Because niche-constructing traits increase the frequency of higher-fitness environments, selection favors their evolution. Furthermore, their alteration of the actual or experienced environmental distribution creates selective feedback between niche constructing traits and other traits, especially those with genotype-by-environment interaction for fitness. By altering the distribution of experienced environments, niche constructing traits can increase the additive genetic variance for such traits. This effect accelerates the process of overall adaption to the niche-constructed environmental distribution and can contribute to the rapid refinement of alternative phenotypic adaptations to different environments. Our findings suggest that evolutionary biologists revisit and reevaluate the environmental term of the Price Equation: owing to adaptive niche construction, it contributes directly to positive change in mean fitness; its magnitude can be comparable to that of natural selection; and, when there is fitness G × E, it increases the additive genetic variance for fitness, the much-celebrated first term.     

Population genetic variation in genome-wide gene expression

Evolutionary biologists seek to understand which traits display variation, are heritable, and influence differential reproduction, because such traits respond to natural selection and underlie organic evolution. Selection acts upon individual differences within a population. Whether individual differences within a natural population include variation in gene expression levels has not yet been addressed on a genome-wide scale. Here we use DNA microarray technology for measuring comparative gene expression and a refined statistical analysis for the purpose of comparing gene expression levels in natural isolates of the wine yeast Saccharomyces cerevisiae. A method for the Bayesian analysis of gene expression levels is used to compare four natural isolates of S. cerevisiae from Montalcino, Italy. Widespread variation in amino acid metabolism, sulfur assimilation and processing, and protein degradation-primarily consisting of differences in expression level smaller than a factor of 2-is demonstrated. Genetic variation in gene expression among isolates from a natural population is present on a genomic scale. It remains to be determined what role differential gene expression may play in adaptation to new or changing environments.     

Superoxide is a mediator of an altruistic aging program in Saccharomyces cerevisiae

Aging is believed to be a nonadaptive process that escapes the force of natural selection. Here, we challenge this dogma by showing that yeast laboratory strains and strains isolated from grapes undergo an age- and pH-dependent death with features of mammalian programmed cell death (apoptosis). After 90-99% of the population dies, a small mutant subpopulation uses the nutrients released by dead cells to grow. This adaptive regrowth is inversely correlated with protection against superoxide toxicity and life span and is associated with elevated age-dependent release of nutrients and increased mutation frequency. Computational simulations confirm that premature aging together with a relatively high mutation frequency can result in a major advantage in adaptation to changing environments. These results suggest that under conditions that model natural environments, yeast organisms undergo an altruistic and premature aging and death program, mediated in part by superoxide. The role of similar pathways in the regulation of longevity in organisms ranging from yeast to mice raises the possibility that mammals may also undergo programmed aging.     

Which evolutionary processes influence natural genetic variation for phenotypic traits?

Although many studies provide examples of evolutionary processes such as adaptive evolution, balancing selection, deleterious variation and genetic drift, the relative importance of these selective and stochastic processes for phenotypic variation within and among populations is unclear. Theoretical and empirical studies from humans as well as natural animal and plant populations have made progress in examining the role of these evolutionary forces within species. Tentative generalizations about evolutionary processes across species are beginning to emerge, as well as contrasting patterns that characterize different groups of organisms. Furthermore, recent technical advances now allow the combination of ecological measurements of selection in natural environments with population genetic analysis of cloned QTLs, promising advances in identifying the evolutionary processes that influence natural genetic variation.     

Thoughts Toward a Theory of Natural Selection: The Importance of Microbial Experimental Evolution

Natural selection should no longer be thought of simply as a primitive (magical) concept that can be used to support all kinds of evolutionary theorizing. We need to develop causal theories of natural selection; how it arises. Because the factors contributing to the creation of natural selection are expected to be complex and intertwined, theories explaining the causes of natural selection can only be developed through the experimental method. Microbial experimental evolution provides many benefits that using other organisms does not. Microorganisms are small, so millions can be housed in a test tube; they have short generation times, so evolution over hundreds of generations can be easily studied; they can grow in chemically defined media, so the environment can be precisely defined; and they can be frozen, so the fitness of strains or populations can be directly compared across time. Microbial evolution experiments can be divided into two types. The first is to measure the selection coefficient of two known strains over the first 50 or so generations, before advantageous mutations rise to high frequency. This type of experiment can be used to directly test hypotheses. The second is to allow microbial cultures to evolve over many hundreds or thousands of generations and follow the genetic changes, to infer what phenotypes are selected. In the last section of this article, I propose that selection coefficients are not constant, but change as the population becomes fitter, introducing the idea of the selection space.This article is about natural selection. For many years, I have asked my undergraduate students to memorize this definition of natural selection: Natural selection is the differential reproduction and survival of different phenotypes when, at least, part of the differences in phenotypes is caused by differences in genotype. This can also be expressed as differential growth rates of subpopulations when the subpopulations are distinguished by genetic differences. When expressed as differences in the growth rates in terms of the Malthusian growth parameter, m, then natural selection is the difference in birth rates minus the difference in death rates.From demography, we know that birth rates are very variable depending on the environment. In humans in the United States, the birth rate dropped during the economic depression of the 1930s, rose after World War II to produce a baby boom, and dropped afterward. Worldwide, birth rates drop with the provision of government-provided old-age assistance, also with the increasing survival of children previously born. Thus, birth rates are very sensitive to many environmental conditions. Likewise for death rates. We have long known that starvation, disease, war, and fratricide will increase the death rate, often dramatically. There has been a drop in death rates since 1750 as transportation and social organization improved, preventing starvation in local areas as the crops failed. The 1918 flu spiked the death rate and disease could again raise the death rate dramatically. The black plague is famous for wiping out a third to half of some European populations and changing social conditions. Today, high fructose sweetener is blamed for increasing the death rate among lower class Americans. Thus, the environment changes birth and death rates, sometimes dramatically, sometimes very subtly.Turning back to natural selection, natural selection is the difference between two subpopulations, defined by a genetic difference in their birth and death rates weighted by the effects of all environments experienced by these subpopulations over the time period of the observation. Will natural selection be even more complex than population demography or will it be simpler? It could be much more complicated because the response of the birth and death rates of the two subpopulations in the different environments could be different, giving different norms of reaction. Also, the epistasis and dominance could make the reactions of various individuals within each subpopulation to the changing environment very different. Or it could be much simpler when the genetic difference gives different effects only in one environment. For example, continued synthesis of the lactase gene is selected in human populations that ingest lactose as adults.This complexity embedded in the concept of natural selection has been known for a long time. In population genetics, it is assumed that one can estimate an average selection coefficient over all the environments experienced by the population in a set period without needing to specify the environments or their effect on birth and death rates. This selection coefficient is then used to project gene frequency change over time. Because population genetics is interested in the effects or consequences of natural selection, not the causes, it is satisfactory to treat natural selection as a constant without understanding the causes of natural selection. Unfortunately, this simplification has led to a caricature of natural selection as a constant, given a genetic difference.The model of natural selection that I currently use is given in Figure 1. Here, the definition of natural selection as I gave to my students is an expanded definition because phenotypes are generated by genotypes in an environment (the epigenetic environment) and natural selection is generated by differences in phenotypes in an environment (the selective environment). The interaction of genetic variation, epigenetic environment, phenotypic variation, and the selective environment generate natural selection. These are the “causes” of natural selection. The “effects” of natural selection produce changes in allele frequencies giving rise to adaptive evolution. I believe that the most important function of experimental evolution will be to figure out the causal rules or laws of natural selection. I have previously made the analogy of natural selection evolution with force in physics (Dykhuizen 1995). Newton described the effects of force; the understanding of the causes of force were performed over the next 300 years leading to an understanding of electromagnetism, thermodynamics, atomic energy, etc. This understanding has led to most of the practical applications from physics. Hopefully, the same can be performed for natural selection. But, as the causes of force were much stranger than expected, the causes of natural selection will be stranger than we now imagine. Only by doing experiments will we be forced to accept whatever strangeness there is in natural selection.Open in a separate windowFigure 1.The current model of natural selection indicating the complexity of its causes and distinguishing causes from effects. Population genetics studies only the effects of natural selection.     

Adaptation to larval crowding in Drosophila ananassae leads to the evolution of population stability

Density-dependent selection is expected to lead to population stability, especially if r and K tradeoff. Yet, there is no empirical evidence of adaptation to crowding leading to the evolution of stability. We show that populations of Drosophila ananassae selected for adaptation to larval crowding have higher K and lower r, and evolve greater stability than controls. We also show that increased population growth rates at high density can enhance stability, even in the absence of a decrease in r, by ensuring that the crowding adapted populations do not fall to very low sizes. We discuss our results in the context of traits known to have diverged between the selected and control populations, and compare our results with previous work on the evolution of stability in D. melanogaster. Overall, our results suggest that density-dependent selection may be an important factor promoting the evolution of relatively stable dynamics in natural populations.     

A dissection of volatility in yeast

It has been suggested that volatility, the proportion of mutations which change an amino acid, can be used to infer the level of natural selection acting upon a gene. This conjecture is supported by a correlation between volatility and the rate of nonsynonymous substitution (dN), or the ratio of nonsynonymous and synonymous substitution rates, in a variety of organisms. These organisms include yeast, in which the correlations are quite strong. Here we show that these correlations are a by-product of a correlation between synonymous codon bias toward translationally optimal codons and dN. Although this analysis suggests that volatility is not a good measure of the selection, we suggest that it might be possible to infer something about the level of natural selection, from a single genome sequence, using translational codon bias.     

Selection for fitness at the individual or population levels: Modelling effects of genetic modifications in microalgae on productivity and environmental safety

A mechanistic model of microalgae is used to explore the implications of modifying microalgal chlorophyll content and photosynthetic efficiency with an aim to optimising commercial biomass production. The models show the potential for a 10 fold increase in microalgae productivity in genetically modified versus unmodified configurations, while also enabling the use of bioreactors of greater optical depth operating at lower dilution rates. Analysis suggests that natural selection of a trait benefiting the individual (high Chl:C_max, i.e., high antennae size) conflicts with artificial selection of a trait (low Chl:C_max) of most benefit to production at the population level. The implication is that GM strains rather than strains selected from nature will be most beneficial for commercial algal biofuels production. Further, escaped GM algae populations may, depending on the specific nature of the modification, be quickly out-competed by the natural forms because individually a high Chl:C is beneficial in low light environments. However, it remains possible that changes in biochemical composition associated with genetic modification of photosystem competence, or with other selection processes to enhance commercial gain, may adversely affect the value of such organisms as prey for zooplankton, leading to the unwanted generation of future harmful algae.     

Population history and natural selection shape patterns of genetic variation in 132 genes

Identifying regions of the human genome that have been targets of natural selection will provide important insights into human evolutionary history and may facilitate the identification of complex disease genes. Although the signature that natural selection imparts on DNA sequence variation is difficult to disentangle from the effects of neutral processes such as population demographic history, selective and demographic forces can be distinguished by analyzing multiple loci dispersed throughout the genome. We studied the molecular evolution of 132 genes by comprehensively resequencing them in 24 African-Americans and 23 European-Americans. We developed a rigorous computational approach for taking into account multiple hypothesis tests and demographic history and found that while many apparent selective events can instead be explained by demography, there is also strong evidence for positive or balancing selection at eight genes in the European-American population, but none in the African-American population. Our results suggest that the migration of modern humans out of Africa into new environments was accompanied by genetic adaptations to emergent selective forces. In addition, a region containing four contiguous genes on Chromosome 7 showed striking evidence of a recent selective sweep in European-Americans. More generally, our results have important implications for mapping genes underlying complex human diseases.     

Fitness effects of mutations in bacteria

Mutation is the primary source of variation in any organism. Without it, natural selection cannot operate and organisms cannot adapt to novel environments. Mutation is also generally a source of defect: many mutations are not neutral but cause fitness decreases in the organisms where they arise. In bacteria, another important source of variation is horizontal gene transfer. This source of variation can also cause beneficial or deleterious effects. Determining the distribution of fitness effects of mutations in different environments and genetic backgrounds is an active research field. In bacteria, knowledge of these distributions is key for understanding important traits. For example, for determining the dynamics of microorganisms with a high genomic mutation rate (mutators), and for understanding the evolution of antibiotic resistance, and the emergence of pathogenic traits. All of these characteristics are extremely relevant for human health both at the individual and population levels. Experimental evolution has been a valuable tool to address these questions. Here, we review some of the important findings of mutation effects in bacteria revealed through laboratory experiments.     

Ancestrality and evolution of trait syndromes in finches (Fringillidae)

Species traits have been hypothesized by one of us (Ponge, 2013) to evolve in a correlated manner as species colonize stable, undisturbed habitats, shifting from “ancestral” to “derived” strategies. We predicted that generalism, r‐selection, sexual monomorphism, and migration/gregariousness are the ancestral states (collectively called strategy A) and evolved correlatively toward specialism, K‐selection, sexual dimorphism, and residence/territoriality as habitat stabilized (collectively called B strategy). We analyzed the correlated evolution of four syndromes, summarizing the covariation between 53 traits, respectively, involved in ecological specialization, r‐K gradient, sexual selection, and dispersal/social behaviors in 81 species representative of Fringillidae, a bird family with available natural history information and that shows variability for all these traits. The ancestrality of strategy A was supported for three of the four syndromes, the ancestrality of generalism having a weaker support, except for the core group Carduelinae (69 species). It appeared that two different B‐strategies evolved from the ancestral state A, both associated with highly predictable environments: one in poorly seasonal environments, called B1, with species living permanently in lowland tropics, with “slow pace of life” and weak sexual dimorphism, and one in highly seasonal environments, called B2, with species breeding out‐of‐the‐tropics, migratory, with a “fast pace of life” and high sexual dimorphism.