Populations adapt to fluctuating selection using derived and ancestral allelic diversity

Populations can adapt to changing environments by using allelic diversity, yet whether diversity is recently derived or ancestral is often debated. Although evolution could productively use both types of diversity in a changing environment, their relative frequency has not been quantified. We address this question experimentally using budding yeast strains that harbor a tandem repeat containing URA3 gene, which we expose to cyclical selection and counterselection. We characterize and quantify the dynamics of frameshift events in the URA3 gene in eight populations over 12 cycles of selection and find that ancestral alleles account for 10–20% of all adaptive events. Using a general model of fluctuating selection, we determine how these results depend on mutation rates, population sizes, and fluctuation timescales. We quantify the contribution of derived alleles to the adaptation process using the de novo mutation rate along the population's ancestral lineage, a novel measure that is applicable in a wide range of settings. We find that the adaptive dynamics undergoes a sharp transition from selection on ancestral alleles to selection on derived alleles as fluctuation timescales increase. Our results demonstrate that fluctuations can select between different modes of adaptation over evolutionary timescales.     

Bias in the introduction of variation as an orienting factor in evolution

SUMMARY According to New Synthesis doctrine, the direction of evolution is determined by selection and not by "internal causes" that act by way of propensities of variation. This doctrine rests on the theoretical claim that because mutation rates are small in comparison to selection coefficients, mutation is powerless to overcome opposing selection. Using a simple population-genetic model, this claim is shown to depend on assuming the prior availability of variation, so that mutation may act only as a "pressure" on the frequencies of existing alleles, and not as the evolutionary process that introduces novelty. As shown here, mutational bias in the introduction of novelty can strongly influence the course of evolution, even when mutation rates are small in comparison to selection coefficients. Recognizing this mode of causation provides a distinct mechanistic basis for an "internalist" approach to determining the contribution of mutational and developmental factors to evolutionary phenomena such as homoplasy, parallelism, and directionality.     

The generation of variation and the developmental basis for evolutionary novelty

Organisms exhibit an incredible diversity of form, a fact that makes the evolution of novelty seemingly self-evident. However, despite the "obvious" case for novelty, defining this concept in evolutionary terms is highly problematic, so much so that some have suggested discarding it altogether. Approaches to this problem tend to take either an adaptation- or development-based perspective, but we argue here that an exclusive focus on either of these misses the original intent of the novelty concept and undermines its practical utility. We propose instead that for a feature to be novel, it must have evolved both by a transition between adaptive peaks on the fitness landscape and that this transition must have overcome a previous developmental constraint. This definition focuses novelty on the explanation of apparently difficult or low-probability evolutionary transitions and highlights how the integration of developmental and functional considerations are necessary to evolutionary explanation. It further reinforces that novelty is a central concern not just of evolutionary developmental biology (i.e., "evo-devo") but of evolutionary biology more generally. We explore this definition of novelty in light of four examples that range from the obvious to subtle. J. Exp. Zool. (Mol. Dev. Evol.) 318B:501-517, 2012. ? 2012 Wiley Periodicals, Inc.     

Impact of the terrestrial-aquatic transition on disparity and rates of evolution in the carnivoran skull

Background

Which factors influence the distribution patterns of morphological diversity among clades? The adaptive radiation model predicts that a clade entering new ecological niche will experience high rates of evolution early in its history, followed by a gradual slowing. Here we measure disparity and rates of evolution in Carnivora, specifically focusing on the terrestrial-aquatic transition in Pinnipedia. We analyze fissiped (mostly terrestrial, arboreal, and semi-arboreal, but also including the semi-aquatic otter) and pinniped (secondarily aquatic) carnivorans as a case study of an extreme ecological transition. We used 3D geometric morphometrics to quantify cranial shape in 151 carnivoran specimens (64 fissiped, 87 pinniped) and five exceptionally-preserved fossil pinnipeds, including the stem-pinniped Enaliarctos emlongi. Range-based and variance-based disparity measures were compared between pinnipeds and fissipeds. To distinguish between evolutionary modes, a Brownian motion model was compared to selective regime shifts associated with the terrestrial-aquatic transition and at the base of Pinnipedia. Further, evolutionary patterns were estimated on individual branches using both Ornstein-Uhlenbeck and Independent Evolution models, to examine the origin of pinniped diversity.

Results

Pinnipeds exhibit greater cranial disparity than fissipeds, even though they are less taxonomically diverse and, as a clade nested within fissipeds, phylogenetically younger. Despite this, there is no increase in the rate of morphological evolution at the base of Pinnipedia, as would be predicted by an adaptive radiation model, and a Brownian motion model of evolution is supported. Instead basal pinnipeds populated new areas of morphospace via low to moderate rates of evolution in new directions, followed by later bursts within the crown-group, potentially associated with ecological diversification within the marine realm.

Conclusion

The transition to an aquatic habitat in carnivorans resulted in a shift in cranial morphology without an increase in rate in the stem lineage, contra to the adaptive radiation model. Instead these data suggest a release from evolutionary constraint model, followed by aquatic diversifications within crown families.

Electronic supplementary material

The online version of this article (doi:10.1186/s12862-015-0285-5) contains supplementary material, which is available to authorized users.     

Increased transmission of mutations by low-condition females: evidence for condition-dependent DNA repair

Evidence is mounting that mutation rates are sufficiently high for deleterious alleles to be a major evolutionary force affecting the evolution of sex, the maintenance of genetic variation, and many other evolutionary phenomena. Though point estimates of mutation rates are improving, we remain largely ignorant of the biological factors affecting these rates at the individual level. Of special importance is the possibility that mutation rates are condition-dependent with low-condition individuals experiencing more mutation. Theory predicts that such condition dependence would dramatically increase the rate at which populations adapt to new environments and the extent to which populations suffer from mutation load. Despite its importance, there has been little study of this phenomenon in multicellular organisms. Here, we examine whether DNA repair processes are condition-dependent in Drosophila melanogaster. In this species, damaged DNA in sperm can be repaired by maternal repair processes after fertilization. We exposed high- and low-condition females to sperm containing damaged DNA and then assessed the frequency of lethal mutations on paternally derived X chromosomes transmitted by these females. The rate of lethal mutations transmitted by low-condition females was 30% greater than that of high-condition females, indicating reduced repair capacity of low-condition females. A separate experiment provided no support for an alternative hypothesis based on sperm selection.     

Determinants of simulated RNA evolution

Models of RNA secondary structure folding are widely used to study evolution in theory and simulation. However, systematic studies of the parameters involved are rare. In this paper, we study by simulation how RNA evolution is influenced by three different factors, namely the mutation rate, scaling of the fitness function, and distance measure. We found that for low mutation rates the qualitative evolutionary behavior is robust with respect to the scaling of the fitness function. For efficient mutation rates, which are close to the error threshold, scaling and distance measure have a strong influence on the evolutionary behavior. A global distance measure that takes sequence information additively into account lowers the error threshold. When using a local sequence-structure alignment for the distance, we observed a smoother evolution of the fitness over time. Finally, in addition to the well known error threshold, we identify another threshold of the mutation rate, called divergence threshold, where the qualitative transient behavior changes from a localized to an exploratory search.     

A Model of Genetic Search for Beneficial Mutations: Estimating the Constructive Capacities of Mutagenesis

We attempted to answer the following question: What evolutionary conditions are required to generate novel genetic modules? Our broad formulation of the problem allows us to simultaneously consider such issues as the relationship between the stage of "genetic search" and the rate of adaptive evolution; the theoretical limits to the generative capacities of spontaneous mutagenesis; and the correlation between genome organization and evolvability. We show that adaptive evolution is feasible only when the mutation rate is fine-tuned to a specific range of values and the structures of the genome and genes are optimized in a certain way. Our quantitative analysis has demonstrated that the rate of evolution of novelty depends on several parameters, such as genome size, the length of a module, the size of the adjacent nonfunctional DNA spacers, and the mutation rate at various genomic scales. We evaluated the efficiency of some mechanisms that increase evolvability: bias in the spectrum of mutation rates towards small mutations, and the availability and size of nonfunctional DNA spacers. We show that the probability of successful duplication and insertion of a copy of a functional module increases by several orders of magnitude depending on the length of the spacers flanking the module. We infer that the adaptive evolution of multicellular organisms has become feasible because of the abundance of nonfunctional DNA spacers, particularly introns, in the genome. We also discuss possible reasons underlying evolutionary retention of the mechanisms that increase evolvability.     

A latitudinal gradient in rates of evolution of avian syllable diversity and song length

We ask whether rates of evolution in traits important for reproductive isolation vary across a latitudinal gradient, by quantifying evolutionary rates of two traits important for pre-mating isolation-avian syllable diversity and song length. We analyse over 2500 songs from 116 pairs of closely related New World passerine bird taxa to show that evolutionary rates for the two main groups of passerines-oscines and suboscines-doubled with latitude in both groups for song length. For syllable diversity, oscines (who transmit song culturally) evolved more than 20 times faster at high latitudes than in low latitudes, whereas suboscines (whose songs are innate in most species and who possess very simple song with few syllable types) show no clear latitudinal gradient in rate. Evolutionary rates in oscines and suboscines were similar at tropical latitudes for syllable complexity as well as for song length. These results suggest that evolutionary rates in traits important to reproductive isolation and speciation are influenced by latitude and have been fastest, not in the tropics where species diversity is highest, but towards the poles.     

Does Sex Speed Up Evolutionary Rate and Increase Biodiversity?

Most empirical and theoretical studies have shown that sex increases the rate of evolution, although evidence of sex constraining genomic and epigenetic variation and slowing down evolution also exists. Faster rates with sex have been attributed to new gene combinations, removal of deleterious mutations, and adaptation to heterogeneous environments. Slower rates with sex have been attributed to removal of major genetic rearrangements, the cost of finding a mate, vulnerability to predation, and exposure to sexually transmitted diseases. Whether sex speeds or slows evolution, the connection between reproductive mode, the evolutionary rate, and species diversity remains largely unexplored. Here we present a spatially explicit model of ecological and evolutionary dynamics based on DNA sequence change to study the connection between mutation, speciation, and the resulting biodiversity in sexual and asexual populations. We show that faster speciation can decrease the abundance of newly formed species and thus decrease long-term biodiversity. In this way, sex can reduce diversity relative to asexual populations, because it leads to a higher rate of production of new species, but with lower abundances. Our results show that reproductive mode and the mechanisms underlying it can alter the link between mutation, evolutionary rate, speciation and biodiversity and we suggest that a high rate of evolution may not be required to yield high biodiversity.     

Evolutionary dynamics of human retroviruses investigated through full-genome scanning

To test hypotheses on the differences in retroviral genetic diversity, we compared the evolutionary dynamics of the human immunodeficiency virus type 1 (HIV-1) group M and the primate T-cell lymphotropic virus (PTLV) using a full-genome analysis. Evolutionary rates and nonsynonymous/synonymous substitution rate ratios were estimated across the genome using a maximum likelihood sliding window approach, and molecular clock properties were investigated. We confirm a remarkable difference in genetic stability and selective pressure at the interhost level. While there is evidence for adaptive evolution in HIV-1, the evolution of PTLV is almost exclusively characterized by negative selection or nearly neutral processes. For both retroviruses, evolutionary rate estimates across the genome reflect the differential selective constraints. However, based on the relationship between evolutionary rate and selective pressure and based on the comparison of synonymous substitution rates, the differences in rate between HIV-1 and PTLV cannot be explained by selective forces only. Several evolutionary and statistical assumptions, examined using a Bayesian coalescent method, were shown to have little influence on our inference.     

Conceptualizing evolutionary novelty: moving beyond definitional debates

According to many biologists, explaining the evolution of morphological novelty and behavioral innovation are central endeavors in contemporary evolutionary biology. These endeavors are inherently multidisciplinary but also have involved a high degree of controversy. One key source of controversy is the definitional diversity associated with the concept of evolutionary novelty, which can lead to contradictory claims (a novel trait according to one definition is not a novel trait according to another). We argue that this diversity should be interpreted in light of a different epistemic role played by the concept of evolutionary novelty-the structuring of a problem space or setting of an explanatory agenda-rather than the concept's capacity to categorize traits as novel. This distinctive role is consistent with the definitional diversity and shows that the concept of novelty benefits ongoing investigation by focusing attention on answering different questions related to comprehending the origins of novelty. A review of recent theoretical and empirical work on evolutionary novelty confirms this interpretation. J. Exp. Zool. (Mol. Dev. Evol.) 318B:417-427, 2012. ? 2012 Wiley Periodicals, Inc.     

A multidimensional framework for measuring biotic novelty: How novel is a community?

Anthropogenic changes in climate, land use, and disturbance regimes, as well as introductions of non‐native species can lead to the transformation of many ecosystems. The resulting novel ecosystems are usually characterized by species assemblages that have not occurred previously in a given area. Quantifying the ecological novelty of communities (i.e., biotic novelty) would enhance the understanding of environmental change. However, quantification remains challenging since current novelty metrics, such as the number and/or proportion of non‐native species in a community, fall short of considering both functional and evolutionary aspects of biotic novelty. Here, we propose the Biotic Novelty Index (BNI), an intuitive and flexible multidimensional measure that combines (a) functional differences between native and non‐native introduced species with (b) temporal dynamics of species introductions. We show that the BNI is an additive partition of Rao's quadratic entropy, capturing the novel interaction component of the community's functional diversity. Simulations show that the index varies predictably with the relative amount of functional novelty added by recently arrived species, and they illustrate the need to provide an additional standardized version of the index. We present a detailed R code and two applications of the BNI by (a) measuring changes of biotic novelty of dry grassland plant communities along an urbanization gradient in a metropolitan region and (b) determining the biotic novelty of plant species assemblages at a national scale. The results illustrate the applicability of the index across scales and its flexibility in the use of data of different quality. Both case studies revealed strong connections between biotic novelty and increasing urbanization, a measure of abiotic novelty. We conclude that the BNI framework may help building a basis for better understanding the ecological and evolutionary consequences of global change.     

Natural selection fails to optimize mutation rates for long-term adaptation on rugged fitness landscapes

The rate of mutation is central to evolution. Mutations are required for adaptation, yet most mutations with phenotypic effects are deleterious. As a consequence, the mutation rate that maximizes adaptation will be some intermediate value. Here, we used digital organisms to investigate the ability of natural selection to adjust and optimize mutation rates. We assessed the optimal mutation rate by empirically determining what mutation rate produced the highest rate of adaptation. Then, we allowed mutation rates to evolve, and we evaluated the proximity to the optimum. Although we chose conditions favorable for mutation rate optimization, the evolved rates were invariably far below the optimum across a wide range of experimental parameter settings. We hypothesized that the reason that mutation rates evolved to be suboptimal was the ruggedness of fitness landscapes. To test this hypothesis, we created a simplified landscape without any fitness valleys and found that, in such conditions, populations evolved near-optimal mutation rates. In contrast, when fitness valleys were added to this simple landscape, the ability of evolving populations to find the optimal mutation rate was lost. We conclude that rugged fitness landscapes can prevent the evolution of mutation rates that are optimal for long-term adaptation. This finding has important implications for applied evolutionary research in both biological and computational realms.     

Population persistence under high mutation rate: From evolutionary rescue to lethal mutagenesis

Populations may genetically adapt to severe stress that would otherwise cause their extirpation. Recent theoretical work, combining stochastic demography with Fisher's geometric model of adaptation, has shown how evolutionary rescue becomes unlikely beyond some critical intensity of stress. Increasing mutation rates may however allow adaptation to more intense stress, raising concerns about the effectiveness of treatments against pathogens. This previous work assumes that populations are rescued by the rise of a single resistance mutation. However, even in asexual organisms, rescue can also stem from the accumulation of multiple mutations in a single genome. Here, we extend previous work to study the rescue process in an asexual population where the mutation rate is sufficiently high so that such events may be common. We predict both the ultimate extinction probability of the population and the distribution of extinction times. We compare the accuracy of different approximations covering a large range of mutation rates. Moderate increase in mutation rates favors evolutionary rescue. However, larger increase leads to extinction by the accumulation of a large mutation load, a process called lethal mutagenesis. We discuss how these results could help design “evolution‐proof” antipathogen treatments that even highly mutable strains could not overcome.     

Similar relative mutation rates in the three genetic compartments of Mesostigma and Chlamydomonas

Levels of nucleotide substitution at silent sites in organelle versus nuclear DNAs have been used to estimate relative mutation rates among these compartments and explain lineage-specific features of genome evolution. Synonymous substitution divergence values in animals suggest that the rate of mutation in the mitochondrial DNA is 10-50 times higher than that of the nuclear DNA, whereas overall data for most seed plants support relative mutation rates in mitochondrial, plastid, and nuclear DNAs of 1:3:10. Little is known about relative mutation rates in green algae, as substitution rate data is limited to only the mitochondrial and nuclear genomes of the chlorophyte Chlamydomonas. Here, we measure silent-site substitution rates in the plastid DNA of Chlamydomonas and the three genetic compartments of the streptophyte green alga Mesostigma. In contrast to the situation in animals and land plants, our results support similar relative mutation rates among the three genetic compartments of both Chlamydomonas and Mesostigma. These data are discussed in relation to published intra-species genetic diversity data for the three genetic compartments of Chlamydomonas and are ultimately used to address contemporary hypotheses on the organelle genome evolution. To guide future work, we describe evolutionary divergence data of all publically available Mesostigma viride strains and identify, for the first time, three distinct lineages of Mesostigma.     

In silico identification of functional divergence between the multiple groEL gene paralogs in Chlamydiae

Background

RNA molecules, through their dual appearance as sequence and structure, represent a suitable model to study evolutionary properties of quasispecies. The essential ingredient in this model is the differentiation between genotype (molecular sequences which are affected by mutation) and phenotype (molecular structure, affected by selection). This framework allows a quantitative analysis of organizational properties of quasispecies as they adapt to different environments, such as their robustness, the effect of the degeneration of the sequence space, or the adaptation under different mutation rates and the error threshold associated.

Results

We describe and analyze the structural properties of molecular quasispecies adapting to different environments both during the transient time before adaptation takes place and in the asymptotic state, once optimization has occurred. We observe a minimum in the adaptation time at values of the mutation rate relatively far from the phenotypic error threshold. Through the definition of a consensus structure, it is shown that the quasispecies retains relevant structural information in a distributed fashion even above the error threshold. This structural robustness depends on the precise shape of the secondary structure used as target of selection. Experimental results available for natural RNA populations are in qualitative agreement with our observations.

Conclusion

Adaptation time of molecular quasispecies to a given environment is optimized at values of the mutation rate well below the phenotypic error threshold. The optimal value results from a trade-off between diversity generation and fixation of advantageous mutants. The critical value of the mutation rate is a function not only of the sequence length, but also of the specific properties of the environment, in this case the selection pressure and the shape of the secondary structure used as target phenotype. Certain functional motifs of RNA secondary structure that withstand high mutation rates (as the ubiquitous hairpin motif) might appear early in evolution and be actually frozen evolutionary accidents.     

A statistical characterization of consistent patterns of human immunodeficiency virus evolution within infected patients

Within-patient HIV populations evolve rapidly because of a high mutation rate, short generation time, and strong positive selection pressures. Previous studies have identified "consistent patterns" of viral sequence evolution. Just before HIV infection progresses to AIDS, evolution seems to slow markedly, and the genetic diversity of the viral population drops. This evolutionary slowdown could be caused either by a reduction in the average viral replication rate or because selection pressures weaken with the collapse of the immune system. The former hypothesis (which we denote "cellular exhaustion") predicts a simultaneous reduction in both synonymous and nonsynonymous evolution, whereas the latter hypothesis (denoted "immune relaxation") predicts that only nonsynonymous evolution will slow. In this paper, we present a set of statistical procedures for distinguishing between these alternative hypotheses using DNA sequences sampled over the course of infection. The first component is a new method for estimating evolutionary rates that takes advantage of the temporal information in longitudinal DNA sequence samples. Second, we develop a set of probability models for the analysis of evolutionary rates in HIV populations in vivo. Application of these models to both synonymous and nonsynonymous evolution affords a comparison of the cellular-exhaustion and immune-relaxation hypotheses. We apply the procedures to longitudinal data sets in which sequences of the env gene were sampled over the entire course of infection. Our analyses (1) statistically confirm that an evolutionary slowdown occurs late in infection, (2) strongly support the immune-relaxation hypothesis, and (3) indicate that the cessation of nonsynonymous evolution is associated with disease progression.     

Integrating micro- and macroevolution of development through the study of horned beetles

A major challenge in evolutionary developmental biology is to understand how developmental evolution on the level of populations and closely related species relates to macroevolutionary transitions and the origin of evolutionary novelty. Here, I review the genetic, developmental, endocrine, and ecological basis of beetle horns, a morphological novelty that exhibits remarkable diversity both below and above the species level. Integrating from a variety of approaches three major insights emerge: the origin of beetle horns relied at least in part on the redeployment of already existing genetic, developmental and endocrine mechanisms. At the same time little to no phylogenetic distance appeared to have been necessary for the evolution of diverse modifier mechanisms that permit substantial modulation of trait expression at different time points during development in different species, sexes, alternative male morphs or even different tissue regions of the same individual. Lastly, at least a subset of these modifier mechanisms can evolve rapidly in geographically isolated populations, apparently driven by relatively simple, and probably ubiquitous, changes in ecological conditions. I discuss the implications of these results for our understanding of the genesis of morphological novelty and diversity.     

Effects of allometry,productivity and lifestyle on rates and limits of body size evolution

Body size affects nearly all aspects of organismal biology, so it is important to understand the constraints and dynamics of body size evolution. Despite empirical work on the macroevolution and macroecology of minimum and maximum size, there is little general quantitative theory on rates and limits of body size evolution. We present a general theory that integrates individual productivity, the lifestyle component of the slow–fast life-history continuum, and the allometric scaling of generation time to predict a clade''s evolutionary rate and asymptotic maximum body size, and the shape of macroevolutionary trajectories during diversifying phases of size evolution. We evaluate this theory using data on the evolution of clade maximum body sizes in mammals during the Cenozoic. As predicted, clade evolutionary rates and asymptotic maximum sizes are larger in more productive clades (e.g. baleen whales), which represent the fast end of the slow–fast lifestyle continuum, and smaller in less productive clades (e.g. primates). The allometric scaling exponent for generation time fundamentally alters the shape of evolutionary trajectories, so allometric effects should be accounted for in models of phenotypic evolution and interpretations of macroevolutionary body size patterns. This work highlights the intimate interplay between the macroecological and macroevolutionary dynamics underlying the generation and maintenance of morphological diversity.     

A Darwinian evolutionary system. I. Definition and basic properties

Biological evolution as conceived by the present synthetic theory of evolution is modelled by a mathematical system which consists of three arrays: the genotype and phenotype population and their environment, and four operators: selection, mutation, recombination, and alteration (describing the change of the environment by the population). An evolutionary process then could be represented as the cyclic iteration of these operations on the respective arrays. Some simple versions of this system were investigated by computer simulation. They exhibited the following properties. (i) Population fitness increased with the generation number. (ii) The evolutionary rate increased with variance of fitness. (iii) The evolutionary rate increased with the number of individuals, and decreased with the number of loci. (iv) The evolutionary rate increased with the selection pressure. (v) For a given system in a given state there existed an optimal mutation rate. (vi) Free recombination was optimal. (vii) The mutational load of fitness increased with the mutation rate, but was independent of the selection pressure; contrary to this, the mutational load of the population “morph” decreased with the selection pressure, i.e. one could compensate for the deleterious effect of mutation by strong selection. These rules applied to haploids with equal, unequal, non-epistatic, and epistatic gene effect, and also to diploids. It was found that epistatic gene effect for relatively low mutation rates slows down evolution, whereas unequal gene effect enhances it. Diploids were not found to be superior to haploids in evolutionary terms, except in the case of diploids with dominant gene action for very small population sizes. The results are discussed with regard to their applicability to the simulation of more complex evolutionary phenomena.