The role of robustness in phenotypic adaptation and innovation

Phenotypes that vary in response to DNA mutations are essential for evolutionary adaptation and innovation. Therefore, it seems that robustness, a lack of phenotypic variability, must hinder adaptation. The main purpose of this review is to show why this is not necessarily correct. There are two reasons. The first is that robustness causes the existence of genotype networks--large connected sets of genotypes with the same phenotype. I discuss why genotype networks facilitate phenotypic variability. The second reason emerges from the evolutionary dynamics of evolving populations on genotype networks. I discuss how these dynamics can render highly robust phenotypes more variable, using examples from protein and RNA macromolecules. In addition, robustness can help avoid an important evolutionary conflict between the interests of individuals and populations-a conflict that can impede evolutionary adaptation.     

ROLE OF SEX AND MIGRATION IN ADAPTATION TO SINK ENVIRONMENTS

Understanding the effects of sex and migration on adaptation to novel environments remains a key problem in evolutionary biology. Using a single‐cell alga Chlamydomonas reinhardtii, we investigated how sex and migration affected rates of evolutionary rescue in a sink environment, and subsequent changes in fitness following evolutionary rescue. We show that sex and migration affect both the rate of evolutionary rescue and subsequent adaptation. However, their combined effects change as the populations adapt to a sink habitat. Both sex and migration independently increased rates of evolutionary rescue, but the effect of sex on subsequent fitness improvements, following initial rescue, changed with migration, as sex was beneficial in the absence of migration but constraining adaptation when combined with migration. These results suggest that sex and migration are beneficial during the initial stages of adaptation, but can become detrimental as the population adapts to its environment.     

Evolutionary genetics of plant adaptation

Plants provide unique opportunities to study the mechanistic basis and evolutionary processes of adaptation to diverse environmental conditions. Complementary laboratory and field experiments are important for testing hypotheses reflecting long-term ecological and evolutionary history. For example, these approaches can infer whether local adaptation results from genetic tradeoffs (antagonistic pleiotropy), where native alleles are best adapted to local conditions, or if local adaptation is caused by conditional neutrality at many loci, where alleles show fitness differences in one environment, but not in a contrasting environment. Ecological genetics in natural populations of perennial or outcrossing plants can also differ substantially from model systems. In this review of the evolutionary genetics of plant adaptation, we emphasize the importance of field studies for understanding the evolutionary dynamics of model and nonmodel systems, highlight a key life history trait (flowering time) and discuss emerging conservation issues.     

EVOLUTIONARY RESPONSES TO ENVIRONMENTAL CHANGES: HOW DOES COMPETITION AFFECT ADAPTATION?

The role and importance of ecological interactions for evolutionary responses to environmental changes is to large extent unknown. Here it is shown that interspecific competition may slow down rates of adaptation substantially and fundamentally change patterns of adaptation to long-term environmental changes. In the model investigated here, species compete for resources distributed along an ecological niche space. Environmental change is represented by a slowly moving resource maximum and evolutionary responses of single species are compared with responses of coalitions of two and three competing species. In scenarios with two and three species, species that are favored by increasing resource availability increase in equilibrium population size whereas disfavored species decline in size. Increased competition makes it less favorable for individuals of a disfavored species to occupy a niche close to the maximum and reduces the selection pressure for tracking the moving resource distribution. Individual-based simulations and an analysis using adaptive dynamics show that the combination of weaker selection pressure and reduced population size reduces the evolutionary rate of the disfavored species considerably. If the resource landscape moves stochastically, weak evolutionary responses cause large fluctuations in population size and thereby large extinction risk for competing species, whereas a single species subject to the same environmental variability may track the resource maximum closely and maintain a much more stable population size. Other studies have shown that competitive interactions may amplify changes in mean population sizes due to environmental changes and thereby increase extinction risks. This study accentuates the harmful role of competitive interactions by illustrating that they may also decrease rates of adaptation. The slowdown in evolutionary rates caused by competition may also contribute to explain low rates of morphological change in spite of large environmental fluctuations found in fossil records.     

Application of heat shock protein expression for detecting natural adaptation and exposure to stress in natural populations

Heat-shock proteins (HSPs) play an undisputed role for maintaining cellular functioning under environmental challenges and protein denaturing conditions. Compelling evidence points to an evolutionary important role of HSPs and a strict evolutionary control of these proteins as a balance between benefits and costs. While there is a great potential for using HSP expression for detecting natural adaptation and exposure to stress in natural populations, some obstacles and key issues await investigation. From an...     

Environmental stress and adaptational responses: consequences for human health outcomes

With the dramatic pace of modernization of the world's population, human adaptation as a theoretical construct and paradigm will likely become a focal scientific issue involving scientists from many disciplinary areas during the 21st Century. Macro and micro environments are in rapid flux and human populations are exposed to rapid change. The concept of adaptation, at least in the field of biological anthropology and human biology, will likely remain tied to evolutionary processes and concepts of selection and fitness. In this paper, we discuss the theoretical constructs of adaptation and adaptability and select three current examples from our ongoing research that involve studies of adaptation and evolutionary processes in modernizing populations in different locations worldwide.     

Evolutionary inevitability of sexual antagonism

Sexual antagonism, whereby mutations are favourable in one sex and disfavourable in the other, is common in natural populations, yet the root causes of sexual antagonism are rarely considered in evolutionary theories of adaptation. Here, we explore the evolutionary consequences of sex-differential selection and genotype-by-sex interactions for adaptation in species with separate sexes. We show that sexual antagonism emerges naturally from sex differences in the direction of selection on phenotypes expressed by both sexes or from sex-by-genotype interactions affecting the expression of such phenotypes. Moreover, modest sex differences in selection or genotype-by-sex effects profoundly influence the long-term evolutionary trajectories of populations with separate sexes, as these conditions trigger the evolution of strong sexual antagonism as a by-product of adaptively driven evolutionary change. The theory demonstrates that sexual antagonism is an inescapable by-product of adaptation in species with separate sexes, whether or not selection favours evolutionary divergence between males and females.     

A practical guide to measuring local adaptation

Patterns of local adaptation are expected to emerge when selection is spatially heterogeneous and sufficiently strong relative to the action of other evolutionary forces. The observation of local adaptation thus provides important insight into evolutionary processes and the adaptive divergence of populations. The detection of local adaptation, however, suffers from several conceptual, statistical and methodological issues. Here, we provide practical recommendations regarding (1) the definition of local adaptation, (2) the analysis of transplant experiments and (3) the optimisation of the experimental design of local adaptation studies. Together, these recommendations provide a unified approach for measuring local adaptation and understanding the adaptive divergence of populations in a wide range of biological systems.     

Proceedings of the SMBE Tri-National Young Investigators' Workshop 2005. Molecular genetics of natural populations

Significant progress in evolutionary genetics has been made by studying, on the one hand, patterns of DNA sequence polymorphism and, on the other, genetic architecture of complex adaptive traits. However, connections between nucleotide variants under selection and adaptively relevant phenotypes are missing. Such connections can be established using precise gene replacement. We review the recent successful introduction of this technique to the analysis of two evolutionarily interesting loci--Odysseus and desaturase2. Both genes have subtle phenotypes that nevertheless could be identified using gene replacement, demonstrating that effects of naturally occurring alleles can be measured in the laboratory. This is an important first step in connecting statistical signatures of selection with adaptation in nature. More candidate genes involved in adaptation, for example, through cloning of genes responsible for reproductive isolation, now need to be identified. Molecular genetic manipulation, DNA polymorphism analysis, and field studies then have to be integrated to provide fresh insights into the mechanisms of evolutionary change.     

Coestimation of recombination,substitution and molecular adaptation rates by approximate Bayesian computation

The estimation of parameters in molecular evolution may be biased when some processes are not considered. For example, the estimation of selection at the molecular level using codon-substitution models can have an upward bias when recombination is ignored. Here we address the joint estimation of recombination, molecular adaptation and substitution rates from coding sequences using approximate Bayesian computation (ABC). We describe the implementation of a regression-based strategy for choosing subsets of summary statistics for coding data, and show that this approach can accurately infer recombination allowing for intracodon recombination breakpoints, molecular adaptation and codon substitution rates. We demonstrate that our ABC approach can outperform other analytical methods under a variety of evolutionary scenarios. We also show that although the choice of the codon-substitution model is important, our inferences are robust to a moderate degree of model misspecification. In addition, we demonstrate that our approach can accurately choose the evolutionary model that best fits the data, providing an alternative for when the use of full-likelihood methods is impracticable. Finally, we applied our ABC method to co-estimate recombination, substitution and molecular adaptation rates from 24 published human immunodeficiency virus 1 coding data sets.     

Does interspecific hybridization influence evolutionary rates? An experimental study of laboratory adaptation in hybrids between Drosophila serrata and Drosophila birchii.

The low initial fitness of progeny from interspecific crosses in animals and the rarity of interspecific hybridization in natural environments have led to a debate about the evolutionary importance of this phenomenon. Here we directly assess the effects of hybridization between Drosophila serrata and Drosophila birchii on evolutionary rates. We looked at the effects on laboratory adaptation over 30 generations in two laboratory environments, one of which involved nutrition and temperature stress. Laboratory adaptation occurred over time in both environments as reflected by a marked change in viability. However, whilst hybrid lines at no stage performed poorly relative to parental lines, their rate of adaptation never exceeded that of the parentals. Thus, there was no evidence that hybridization increased evolutionary rates. Instead, hybrid lines converged phenotypically with one of the parental species.     

Evolutionary conservatism and convergence both lead to striking similarity in ecology,morphology and performance across continents in frogs

Many clades contain ecologically and phenotypically similar species across continents, yet the processes generating this similarity are largely unstudied, leaving fundamental questions unanswered. Is similarity in morphology and performance across assemblages caused by evolutionary convergence or by biogeographic dispersal of evolutionarily conserved ecotypes? Does convergence to new ecological conditions erase evidence of past adaptation? Here, we analyse ecology, morphology and performance in frog assemblages from three continents (Asia, Australia and South America), assessing the importance of dispersal and convergent evolution in explaining similarity across regions. We find three striking results. First, species using the same microhabitat type are highly similar in morphology and performance across both clades and continents. Second, some species on different continents owe their similarity to dispersal and evolutionary conservatism (rather than evolutionary convergence), even over vast temporal and spatial scales. Third, in one case, an ecologically specialized ancestor radiated into diverse ecotypes that have converged with those on other continents, largely erasing traces of past adaptation to their ancestral ecology. Overall, our study highlights the roles of both evolutionary conservatism and convergence in explaining similarity in species traits over large spatial and temporal scales and demonstrates a statistical framework for addressing these questions in other systems.     

Evolutionary-thinking in agricultural weed management

Agricultural weeds evolve in response to crop cultivation. Nevertheless, the central importance of evolutionary ecology for understanding weed invasion, persistence and management in agroecosystems is not widely acknowledged. This paper calls for more evolutionarily-enlightened weed management, in which management principles are informed by evolutionary biology to prevent or minimize weed adaptation and spread. As a first step, a greater knowledge of the extent, structure and significance of genetic variation within and between weed populations is required to fully assess the potential for weed adaptation. The evolution of resistance to herbicides is a classic example of weed adaptation. Even here, most research focuses on describing the physiological and molecular basis of resistance, rather than conducting studies to better understand the evolutionary dynamics of selection for resistance. We suggest approaches to increase the application of evolutionary-thinking to herbicide resistance research. Weed population dynamics models are increasingly important tools in weed management, yet these models often ignore intrapopulation and interpopulation variability, neglecting the potential for weed adaptation in response to management. Future agricultural weed management can benefit from greater integration of ecological and evolutionary principles to predict the long-term responses of weed populations to changing weed management, agricultural environments and global climate.     

Cave-adapted evolution in the North American amblyopsid fishes inferred using phylogenomics and geometric morphometrics

Cave adaptation has evolved repeatedly across the Tree of Life, famously leading to pigmentation and eye degeneration and loss, yet its macroevolutionary implications remain poorly understood. We use the North American amblyopsid fishes, a family spanning a wide degree of cave adaptation, to examine the impact of cave specialization on the modes and tempo of evolution. We reconstruct evolutionary relationships using ultraconserved element loci, estimate the ancestral histories of eye-state, and examine the impact of cave adaptation on body shape evolution. Our phylogenomic analyses provide a well-supported hypothesis for amblyopsid evolutionary relationships. The obligate blind cavefishes form a clade and the cave-facultative eyed spring cavefishes are nested within the obligate cavefishes. Using ancestral state reconstruction, we find support for at least two independent subterranean colonization events within the Amblyopsidae. Eyed and blind fishes have different body shapes, but not different rates of body shape evolution. North American amblyopsids highlight the complex nature of cave-adaptive evolution and the necessity to include multiple lines of evidence to uncover the underlying processes involved in the loss of complex traits.     

Evolution of polygenic traits under global vs local adaptation

Observations about the number, frequency, effect size, and genomic distribution of alleles associated with complex traits must be interpreted in light of evolutionary process. These characteristics, which constitute a trait’s genetic architecture, can dramatically affect evolutionary outcomes in applications from agriculture to medicine, and can provide a window into how evolution works. Here, I review theoretical predictions about the evolution of genetic architecture under spatially homogeneous, global adaptation as compared with spatially heterogeneous, local adaptation. Due to the tension between divergent selection and migration, local adaptation can favor “concentrated” genetic architectures that are enriched for alleles of larger effect, clustered in a smaller number of genomic regions, relative to expectations under global adaptation. However, the evolution of such architectures may be limited by many factors, including the genotypic redundancy of the trait, mutation rate, and temporal variability of environment. I review the circumstances in which predictions differ for global vs local adaptation and discuss where progress can be made in testing hypotheses using data from natural populations and lab experiments. As the field of comparative population genomics expands in scope, differences in architecture among traits and species will provide insights into how evolution works, and such differences must be interpreted in light of which kind of selection has been operating.     

Adaptive evolution in invasive species

Many emerging invasive species display evidence of rapid adaptation. Contemporary genetic studies demonstrate that adaptation to novel environments can occur within 20 generations or less, indicating that evolutionary processes can influence invasiveness. However, the source of genetic or epigenetic variation underlying these changes remains uncharacterised. Here, we review the potential for rapid adaptation from standing genetic variation and from new mutations, and examine four types of evolutionary change that might promote or constrain rapid adaptation during the invasion process. Understanding the source of variation that contributes to adaptive evolution in invasive plants is important for predicting future invasion scenarios, identifying candidate genes involved in invasiveness, and, more generally, for understanding how populations can evolve rapidly in response to novel and changing environments.     

Evolution of leaf form correlates with tropical-temperate transitions in Viburnum (Adoxaceae)

Strong latitudinal patterns in leaf form are well documented in floristic comparisons and palaeobotanical studies. However, there is little agreement about their functional significance; in fact, it is still unknown to what degree these patterns were generated by repeated evolutionary adaptation. We analysed leaf form in the woody angiosperm clade Viburnum (Adoxaceae) and document evolutionarily correlated shifts in leafing habit, leaf margin morphology, leaf shape and climate. Multiple independent shifts between tropical and temperate forest habitats have repeatedly been accompanied by a change between evergreen, elliptical leaves with entire margins and deciduous, more rounded leaves with toothed or lobed margins. These consistent shifts in Viburnum support repeated evolutionary adaptation as a major determinant of the global correlation between leaf form and mean annual temperature. Our results provide a new theoretical grounding for the inference of past climates using fossil leaf assemblages.     

Limits to adaptation in asexual populations

In asexual populations, the rate of adaptation is basically limited by the frequency and properties of spontaneous beneficial mutations. Hence, knowledge of these mutational properties and how they are affected by particular evolutionary conditions is a precondition for understanding the process of adaptation. Here, we address how the rate of adaptation of asexual populations is limited by its population size and mutation rate, as well as by two factors affecting the fraction of mutations that confer a benefit, i.e. the initial adaptedness of the population and the variability of the environment. These factors both influence which mutations are likely to occur, as well as the probability that they will ultimately contribute to adaptation. We attempt to separate the consequences of these basic population features in terms of their effect on the rate of adaptation by using results from evolution experiments with microorganisms.     

中国榕小蜂触角感受器形态特征及进化适应性分析

【目的】榕树与传粉榕小蜂体系是协同进化、专性传粉的经典系统,每种榕树上一般还生活有种类丰富、数目众多的非传粉榕小蜂。在选择压力下,榕小蜂为在榕果内生存产生了明显的适应性形态。触角感受器是昆虫通讯系统的单元,其形态是反映生态和进化适应性的最佳特征之一。本文旨在对中国部分传粉和非传粉榕小蜂的触角感受器的形态多样性和进化适应性进行系统研究。【方法】对来源于海南和云南15种榕树上24种榕小蜂54个型的触角感受器形态进行了扫描电镜观察,基于现有的分子系统发育树,对传粉榕小蜂触角感受器的形态特征进行了性状演化分析,并对榕小蜂的形态特征进行了进化适应性分析。【结果】榕小蜂触角感受器普遍存在雌雄二型现象。雌蜂触角感受器种类有毛状、锥状、板状、刺状、钟形、腔锥状和栓锥状等,数目丰富,并且进果产卵的传粉雌蜂和果外产卵的非传粉雌蜂之间、进果产卵的传粉雌蜂和进果产卵的非传粉雌蜂之间在形态上存在差异。传粉雄蜂和不具有雄性多型现象的非传粉雄蜂触角感受器极为退化,具有雄性多型的非传粉雄蜂触角感受器形态在种内不具有显著差异。性状演化分析表明进化路径相当复杂,可能存在多次独立进化过程。触角感受器的形态类型与其进化适应性相关。【结论】榕小蜂触角感受器类型多样,形态变化丰富,并为适应榕果内的生存而产生了进化适应性特点。雌蜂和雄蜂在榕果内受到了完全不同的选择压力,行使不同的生态功能,从而产生了不同的适应性形态。不同的适应性形态可能与雌蜂不同的产卵行为、雄蜂不同的交配策略具有一定联系。该文是首次对中国榕小蜂触角感受器形态进行系统研究的报道,有助于更好地理解榕小蜂的形态特征、进化路线、行为策略和生态关系。