Genetics, development and evolution of adaptive pigmentation in vertebrates

The study of pigmentation has played an important role in the intersection of evolution, genetics, and developmental biology. Pigmentation's utility as a visible phenotypic marker has resulted in over 100 years of intense study of coat color mutations in laboratory mice, thereby creating an impressive list of candidate genes and an understanding of the developmental mechanisms responsible for the phenotypic effects. Variation in color and pigment patterning has also served as the focus of many classic studies of naturally occurring phenotypic variation in a wide variety of vertebrates, providing some of the most compelling cases for parallel and convergent evolution. Thus, the pigmentation model system holds much promise for understanding the nature of adaptation by linking genetic changes to variation in fitness-related traits. Here, I first discuss the historical role of pigmentation in genetics, development and evolutionary biology. I then discuss recent empirically based studies in vertebrates, which rely on these historical foundations to make connections between genotype and phenotype for ecologically important pigmentation traits. These studies provide insight into the evolutionary process by uncovering the genetic basis of adaptive traits and addressing such long-standing questions in evolutionary biology as (1) are adaptive changes predominantly caused by mutations in regulatory regions or coding regions? (2) is adaptation driven by the fixation of dominant mutations? and (3) to what extent are parallel phenotypic changes caused by similar genetic changes? It is clear that coloration has much to teach us about the molecular basis of organismal diversity, adaptation and the evolutionary process.     

Playing Darwin. Part B. 20 years of domestication in Drosophila subobscura

Adaptation to a new environment (as well as its underlying mechanisms) is one of the most important topics in Evolutionary Biology. Understanding the adaptive process of natural populations to captivity is essential not only in general evolutionary studies but also in conservation programmes. Since 1990, the Group of Experimental Evolution (CBA/FCUL) has been performing long-term, real-time evolutionary studies, with the characterization of laboratory adaptation in populations of Drosophila subobscura founded in different times and from different locations. Initially, these experiments involved phenotypic assays and more recently were expanded to studies at the molecular level (microsatellite and chromosomal polymorphisms) and with different population sizes. Throughout these two decades, a clear pattern of evolutionary convergence to long-established laboratory populations has been consistently observed in several life-history traits. However, contingencies across foundations were also found during the adaptive process. In characters with complex evolutionary trajectories, the data suggested that the comparative method lacked predictive capacity relative to real-time evolutionary trajectories (experimental evolution). Microsatellite analysis revealed general similarity in gene diversity and allele number between studied populations, as well as an unclear association between genetic variability and evolutionary potential. Nevertheless, ongoing studies in all foundations are being carried out to further test this hypothesis. A comparison between recently introduced and long-term populations (founded from the same natural location) has shown higher degree of chromosomal polymorphism in recent ones. Finally, our findings suggest higher heterogeneity between small-sized populations, as well as a slower evolutionary rate in characters close to fitness (such as fecundity and mating behaviour). This comprehensive study is aimed at better understanding the processes and patterns underlying adaptation to captivity, as well as its genetic basis.     

The genetic basis of thermal reaction norm evolution in lab and natural phage populations

Two major goals of laboratory evolution experiments are to integrate from genotype to phenotype to fitness, and to understand the genetic basis of adaptation in natural populations. Here we demonstrate that both goals are possible by re-examining the outcome of a previous laboratory evolution experiment in which the bacteriophage G4 was adapted to high temperatures. We quantified the evolutionary changes in the thermal reaction norms—the curves that describe the effect of temperature on the growth rate of the phages—and decomposed the changes into modes of biological interest. Our analysis indicated that changes in optimal temperature accounted for almost half of the evolutionary changes in thermal reaction norm shape, and made the largest contribution toward adaptation at high temperatures. Genome sequencing allowed us to associate reaction norm shape changes with particular nucleotide mutations, and several of the identified mutations were found to be polymorphic in natural populations. Growth rate measures of natural phage that differed at a site that contributed substantially to adaptation in the lab indicated that this mutation also underlies thermal reaction norm shape variation in nature. In combination, our results suggest that laboratory evolution experiments may successfully predict the genetic bases of evolutionary responses to temperature in nature. The implications of this work for viral evolution arise from the fact that shifts in the thermal optimum are characterized by tradeoffs in performance between high and low temperatures. Optimum shifts, if characteristic of viral adaptation to novel temperatures, would ensure the success of vaccine development strategies that adapt viruses to low temperatures in an attempt to reduce virulence at higher (body) temperatures.     

Genetic correlation in relation to differences in dosage of a stressor

We exposed the strains of Chlamydomonas isolated from an outbred laboratory population to a range of concentrations of salt (NaCl) up to an extirpative level that the base population could not tolerate. The genetic variance of yield increased with stress over the first half of this range before collapsing to nearly zero. The genetic correlation decreased with environmental distance, whether measured as a difference in dosage or as an environmental variance. This result is consistent with previous studies and provides a basis for interpreting adaptation to a deteriorating environment and the process of evolutionary rescue.     

Mimulus is an emerging model system for the integration of ecological and genomic studies

The plant genus Mimulus is rapidly emerging as a model system for studies of evolutionary and ecological functional genomics. Mimulus contains a wide array of phenotypic, ecological and genomic diversity. Numerous studies have proven the experimental tractability of Mimulus in laboratory and field studies. Genomic resources currently under development are making Mimulus an excellent system for determining the genetic and genomic basis of adaptation and speciation. Here, we introduce some of the phenotypic and genetic diversity in the genus Mimulus and highlight how direct genetic studies with Mimulus can address a wide spectrum of ecological and evolutionary questions. In addition, we present the genomic resources currently available for Mimulus and discuss future directions for research. The integration of ecology and genetics with bioinformatics and genome technology offers great promise for exploring the mechanistic basis of adaptive evolution and the genetics of speciation.     

The evolution of quantitative traits in complex environments

Species inhabit complex environments and respond to selection imposed by numerous abiotic and biotic conditions that vary in both space and time. Environmental heterogeneity strongly influences trait evolution and patterns of adaptive population differentiation. For example, heterogeneity can favor local adaptation, or can promote the evolution of plastic genotypes that alter their phenotypes based on the conditions they encounter. Different abiotic and biotic agents of selection can act synergistically to either accelerate or constrain trait evolution. The environmental context has profound effects on quantitative genetic parameters. For instance, heritabilities measured in controlled conditions often exceed those measured in the field; thus, laboratory experiments could overestimate the potential for a population to respond to selection. Nevertheless, most studies of the genetic basis of ecologically relevant traits are conducted in simplified laboratory environments, which do not reflect the complexity of nature. Here, we advocate for manipulative field experiments in the native ranges of plant species that differ in mating system, life-history strategy and growth form. Field studies are vital to evaluate the roles of disparate agents of selection, to elucidate the targets of selection and to develop a nuanced perspective on the evolution of quantitative traits. Quantitative genetics field studies will also shed light on the potential for natural populations to adapt to novel climates in highly fragmented landscapes. Drawing from our experience with the ecological model system Boechera (Brassicaceae), we discuss advancements possible through dedicated field studies, highlight future research directions and examine the challenges associated with field studies.     

How enzymes adapt: lessons from directed evolution

Enzymes that are adapted to widely different temperature niches are being used to investigate the molecular basis of protein stability and enzyme function. However, natural evolution is complex: random noise, historical accidents and ignorance of the selection pressures at work during adaptation all cloud comparative studies. Here, we review how adaptation in the laboratory by directed evolution can complement studies of natural enzymes in the effort to understand stability and function. Laboratory evolution experiments can attempt to mimic natural evolution and identify different adaptive mechanisms. However, laboratory evolution might make its biggest contribution in explorations of nonnatural functions, by allowing us to distinguish the properties nutured by evolution from those dictated by the laws of physical chemistry.     

HOW REPEATABLE IS ADAPTIVE EVOLUTION? THE ROLE OF GEOGRAPHICAL ORIGIN AND FOUNDER EFFECTS IN LABORATORY ADAPTATION

The importance of contingency versus predictability in evolution has been a long-standing issue, particularly the interaction between genetic background, founder effects, and selection. Here we address experimentally the effects of genetic background and founder events on the repeatability of laboratory adaptation in Drosophila subobscura populations for several functional traits. We found disparate starting points for adaptation among laboratory populations derived from independently sampled wild populations for all traits. With respect to the subsequent evolutionary rate during laboratory adaptation, starvation resistance varied considerably among foundations such that the outcome of laboratory evolution is rather unpredictable for this particular trait, even in direction. In contrast, the laboratory evolution of traits closely related to fitness was less contingent on the circumstances of foundation. These findings suggest that the initial laboratory evolution of weakly selected characters may be unpredictable, even when the key adaptations under evolutionary domestication are predictable with respect to their trajectories.     

Adaptation of a South American malaria vector to laboratory colonization suggests faster-male evolution for mating ability

Background  

Anopheles (Nyssorhynchus) albitarsis (Diptera: Culicidae) is one of the very few South American mosquito vectors of malaria successfully colonized in the laboratory. These vectors are very hard to breed because they rarely mate in artificial conditions. A few years ago a free-mating laboratory colony of An. albitarsis sensu stricto was established after about 30 generations of artificial-mating. To begin to understand the process of adaptation of these malaria vectors to the laboratory we have compared the insemination rates of colony mosquitoes to those from the original population in both artificial and free-mating crosses. We also carried out crossing experiments between the two types of mosquitoes for a preliminary analysis of the genetic basis of such adaptation.     

Variation in the rate of convergent evolution: adaptation to a laboratory environment in Drosophila subobscura

Adaptation to novel environments is a central issue in evolutionary biology. One important question is the prevalence of convergence when different populations adapt to the same or similar environments. We investigated this by comparing two studies, 6 years apart, of laboratory adaptation of populations of Drosophila subobscura founded from the same natural location. In both studies several life‐history traits were periodically assayed for the first 14 generations of laboratory adaptation, as well as later generations, and compared with established, laboratory, control populations. The results indicated: (1) a process of convergence for all traits; (2) differences between the two studies in the pattern and rate of convergence; (3) dependence of the evolutionary rates on initial differentiation. The differences between studies might be the result of the differences in the founder populations and/or changes in the lab environment. In either case, the results suggest that microevolution is highly sensitive to genetic and environmental conditions.     

Canalization breakdown and evolution in a source-sink system

Understanding the process of adaptation to novel environments may help to elucidate several ecological phenomena, from the stability of species range margins to host-pathogen specificity and persistence in degraded habitats. We study evolution in one type of novel environment: a sink habitat where populations cannot persist without recurrent immigration from a source population. Previous studies on source-sink evolution have focused on how extrinsic environmental factors influence adaptation to a sink, but few studies have examined how intrinsic genetic factors influence adaptation. We use an individual-based model to explore how genetic canalization that evolves in gene regulation networks influences the adaptation of a population to a sink. We find that as canalization in the regulation network increases, the probability of adaptation to the novel habitat decreases. When adaptation to the habitat does occur, it is usually preceded by a breakdown of canalization. As evolution continues in the novel habitat, canalization reemerges, but a legacy of the breakdown may remain, even after several generations. We also find that environmental noise tends to increase the probability of adaptation to the novel habitat. Our results suggest that the details of genetic architecture can significantly influence the likelihood of niche evolution in novel environments.     

Predicting evolution from genomics: experimental evolution of bacteriophage T7

A wealth of molecular biology has been exploited in designing and interpreting experimental evolution studies with bacteriophage T7. The modest size of its genome (40 kb dsDNA) and the ease of making genetic constructs, combined with the many genetic resources for its host (Escherichia coli), have enabled comprehensive and detailed studies of experimental adaptations. In several studies, the genome was specifically altered (gene knockouts, gene replacements, reordering of genetic elements) such that a priori knowledge of genetics and biochemistry of the phage could be used to predict the pathways of compensatory evolution when the modified phage is adapted to recover fitness. In other work, the phage has been adapted to specific environmental conditions chosen to select phenotypic outcomes with a quantitative basis, and the molecular bases of that evolution have been explored. Predicting the outcomes of these adaptations has been challenging. In hindsight, one-third to one-half of the compensatory nucleotide changes observed during the adaptation can be rationalized based on T7 biology. This rationalization usually only applies at the genetic level-a gene product may be known to be involved in the affected pathway, but it usually remains unknown how the observed change affects activity. The progress is encouraging, but the prediction of experimental evolution pathways remains far from complete, and is still sometimes confounded by observation when an adaptation yields a completely unexpected outcome.     

Ethanol resistance in Drosophila melanogaster has increased in parallel cold‐adapted populations and shows a variable genetic architecture within and between populations

Understanding the genetic properties of adaptive trait evolution is a fundamental crux of biological inquiry that links molecular processes to biological diversity. Important uncertainties persist regarding the genetic predictability of adaptive trait change, the role of standing variation, and whether adaptation tends to result in the fixation of favored variants. Here, we use the recurrent evolution of enhanced ethanol resistance in Drosophila melanogaster during this species’ worldwide expansion as a promising system to add to our understanding of the genetics of adaptation. We find that elevated ethanol resistance has evolved at least three times in different cooler regions of the species’ modern range—not only at high latitude but also in two African high‐altitude regions. Applying a bulk segregant mapping framework, we find that the genetic architecture of ethanol resistance evolution differs substantially not only between our three resistant populations, but also between two crosses involving the same European population. We then apply population genetic scans for local adaptation within our quantitative trait locus regions, and we find potential contributions of genes with annotated roles in spindle localization, membrane composition, sterol and alcohol metabolism, and other processes. We also apply simulation‐based analyses that confirm the variable genetic basis of ethanol resistance and hint at a moderately polygenic architecture. However, these simulations indicate that larger‐scale studies will be needed to more clearly quantify the genetic architecture of adaptive evolution and to firmly connect trait evolution to specific causative loci.     

Extent of QTL Reuse During Repeated Phenotypic Divergence of Sympatric Threespine Stickleback

How predictable is the genetic basis of phenotypic adaptation? Answering this question begins by estimating the repeatability of adaptation at the genetic level. Here, we provide a comprehensive estimate of the repeatability of the genetic basis of adaptive phenotypic evolution in a natural system. We used quantitative trait locus (QTL) mapping to discover genomic regions controlling a large number of morphological traits that have diverged in parallel between pairs of threespine stickleback (Gasterosteus aculeatus species complex) in Paxton and Priest lakes, British Columbia. We found that nearly half of QTL affected the same traits in the same direction in both species pairs. Another 40% influenced a parallel phenotypic trait in one lake but not the other. The remaining 10% of QTL had phenotypic effects in opposite directions in the two species pairs. Similarity in the proportional contributions of all QTL to parallel trait differences was about 0.4. Surprisingly, QTL reuse was unrelated to phenotypic effect size. Our results indicate that repeated use of the same genomic regions is a pervasive feature of parallel phenotypic adaptation, at least in sticklebacks. Identifying the causes of this pattern would aid prediction of the genetic basis of phenotypic evolution.     

Ecologically relevant stress resistance: from microarrays and quantitative trait loci to candidate genes — A research plan and preliminary results using<Emphasis Type="Italic">Drosophila</Emphasis> as a model organism and climatic and genetic stress as model stresses

We aim at studying adaptation to genetic and environmental stress and its evolutionary implications at different levels of biological organization. Stress influences cellular processes, individual physiology, genetic variation at the population level, and the process of natural selection. To investigate these highly connected levels of stress effects, it is advisable - if not critical - to integrate approaches from ecology, evolution, physiology, molecular biology and genetics. To investigate the mechanisms of stress resistance, how resistance evolves, and what factors contribute to and constrain its evolution, we use the well-defined model systems ofDrosophila species, representing both cosmopolitan species such asD. melanogaster with a known genome map, and more specialized and ecologically well described species such as the cactophilicD. buzzatii. Various climate-related stresses are used as model stresses including desiccation, starvation, cold and heat. Genetic stress or genetic load is modelled by studying the consequences of inbreeding, the accumulation of (slightly) deleterious mutations, hybridization or the loss of genetic variability. We present here a research plan and preliminary results combining various approaches: molecular techniques such as microarrays, quantitative trait loci (QTL) analyses, quantitative PCR, ELISA or Western blotting are combined with population studies of resistance to climatic and genetic stress in natural populations collected across climatic gradients as well as in selection lines maintained in the laboratory.     

Molecular Mechanisms of Stress Adaptation in Plant Natural Populations

Recent advances in studies of genetic variation at protein and DNA levels in plant natural populations and its relationship with environmental changes were reviewed with special reference to the works on the wild barley ( Hordeum spontaneum C. Koch.). On one side, adaptation was shown in statistic data, on the other side, the fact that a considerable part of genetic variation does exist within populations (subpopulations) under same ecological condition indicated its maintainability of neutral or near-neutral mutations in natural populations. The researches on adaptive populations of plants, especially on wild soybean ( Glycine soja Sieb. et Zucc.) mainly conducted in author's laboratory, have shown that the most part of molecular variation within and among populations can not be explained by selection particularly as far as the individual uniqueness was concerned. There are some data shown that adaptation may be caused by accumulation of a few near-neutral mutations. Recent publications on molecular mechanisms of morphological evolution has been received special attention to elucidate the discrepancy between molecular evolution and morphological adaptive evolution. A frame on the unified evolution theory has been built. Finally some related viewpoints of philosophy were discussed.     

植物自然群体适应逆境的分子机理

Recent advances in studies of genetic variation at protein andDNA levels in plant natural populations and its relationship with environmental changes were reviewed with special reference to the works on the wild barley (Hordeum spontaneum C. Koch.). On one side, adaptation was shown in statistic data, on the other side, the fact that a considerable part of genetic variation does exist within populations (subpopulations) under same ecological condition indicated its maintainability of neutral or near-neutral mutations in natural populations. The researches on adaptive populations of plants, especially on wild soybean (Glycine soja Sieb. et Zucc.) mainly conducted in author's laboratory, have shown that the most part of molecular variation within and among populations can not be explained by selection particularly as far as the individual uniqueness was concerned. There are some data shown that adaptation may be caused by accumulation of a few near-neutral mutations. Recent publications on molecular mechanisms of morphological evolution has been received special attention to elucidate the discrepancy between molecular evolution and morphological adaptive evolution. A frame on the unified evolution theory has been built. Finally some related viewpoints of philosophy were discussed.     

Biological pathways to adaptability--interactions between genome, epigenome, nervous system and environment for adaptive behavior

Because living systems depend on their environment, the evolution of environmental adaptability is inseparable from the evolution of life itself (Pross 2003). In animals and humans, environmental adaptability extends further to adaptive behavior. It has recently emerged that individual adaptability depends on the interaction of adaptation mechanisms at diverse functional levels. This interaction enables the integration of genetic, epigenetic and environmental factors for coordinated regulation of adaptations. In this review, we first present the basis for the regulation of adaptation mechanisms across functional levels. We then focus on neuronal activity-regulated adaptation mechanisms that involve the regulation of genes, noncoding DNA (ncDNA), ncRNAs and proteins to change the structural and functional properties of neurons. Finally, we discuss a selection of these important neuronal activity-regulated molecules and their effects on brain structure and function and on behavior. Most of the evidence so far is based on sampling of animal tissue or post-mortem studies in humans. However, we also present techniques that combine genetic with behavioral and neurophysiological measures in humans (e.g. genetic imaging) and discuss their potential and limitations. We argue that we need to understand how neuronal activity-dependent adaptation mechanisms integrate genetic, epigenetic and experience-dependent signals in order to explain individual variations in behavior and cognitive performance.     

Evolutionary insight from whole-genome sequencing of experimentally evolved microbes

Experimental evolution (EE) combined with whole‐genome sequencing (WGS) has become a compelling approach to study the fundamental mechanisms and processes that drive evolution. Most EE‐WGS studies published to date have used microbes, owing to their ease of propagation and manipulation in the laboratory and relatively small genome sizes. These experiments are particularly suited to answer long‐standing questions such as: How many mutations underlie adaptive evolution, and how are they distributed across the genome and through time? Are there general rules or principles governing which genes contribute to adaptation, and are certain kinds of genes more likely to be targets than others? How common is epistasis among adaptive mutations, and what does this reveal about the variety of genetic routes to adaptation? How common is parallel evolution, where the same mutations evolve repeatedly and independently in response to similar selective pressures? Here, we summarize the significant findings of this body of work, identify important emerging trends and propose promising directions for future research. We also outline an example of a computational pipeline for use in EE‐WGS studies, based on freely available bioinformatics tools.