Emergent neutrality

Community ecology is in a current state of creative ferment, stimulated by the development of neutral models of community organization. Here, I reflect on recent papers by Scheffer and van Nes, and by Gravel et al., which illuminate how neutrality can emerge from ecological and evolutionary processes, thus suggesting ways to unify neutral and niche perspectives.     

Emergent neutrality drives phytoplankton species coexistence

The mechanisms that drive species coexistence and community dynamics have long puzzled ecologists. Here, we explain species coexistence, size structure and diversity patterns in a phytoplankton community using a combination of four fundamental factors: organism traits, size-based constraints, hydrology and species competition. Using a 'microscopic' Lotka-Volterra competition (MLVC) model (i.e. with explicit recipes to compute its parameters), we provide a mechanistic explanation of species coexistence along a niche axis (i.e. organismic volume). We based our model on empirically measured quantities, minimal ecological assumptions and stochastic processes. In nature, we found aggregated patterns of species biovolume (i.e. clumps) along the volume axis and a peak in species richness. Both patterns were reproduced by the MLVC model. Observed clumps corresponded to niche zones (volumes) where species fitness was highest, or where fitness was equal among competing species. The latter implies the action of equalizing processes, which would suggest emergent neutrality as a plausible mechanism to explain community patterns.     

Heritable genetic variation and potential for adaptive evolution in asexual aphids (Aphidoidea)

Aphid life cycles can encompass cyclical parthenogenesis, obligate parthenogenesis, obligate parthenogenesis with male production and an intermediate 'bet-hedging' strategy where an aphid genotype will over-winter by continuing to reproduce by parthenogenesis and by investment in sexually produced eggs. In this paper, we focus on aphid lineages that reproduce entirely parthenogenetically (asexual aphids), in contrast to those that have any sexual forms in the annual cycle. Using modern molecular techniques, aphid biologists have made many empirical observations showing that asexual lineages are widespread both geographically and temporally. Indeed, we are collectively beginning to gather data on the evolution and persistence of these lineages through time. Here we review aphid karyology and parthenogenesis, both essential for interpretation of the molecular and ecological evolution of aphid asexual lineages. We describe the growing list of studies that have identified aphid genotypes that are both temporally and geographically widespread. We then collate examples of molecular and chromosomal evolution in asexual aphids and review the literature pertaining to phenotypic evolution and ecological diversification of asexual aphid lineages. In addition, we briefly discuss the potential of bacterial endosymbionts and epigenetic effects to influence the evolution of asexual aphid lineages. Lastly we provide a list of aphid taxa believed to be obligately asexual. This will be a useful resource for those seeking parthenogenetic animals as study systems. In conclusion, we present guidelines for the use of the term clone in aphid biology and stress the need for well-designed and well-executed studies examining the potential of asexual aphid lineages for adaptive evolution.  © 2003 The Linnean Society of London. Biological Journal of the Linnean Society , 2003, 79 , 115–135.     

Reconciling niche and neutrality through the Emergent Group approach

Both niche and neutral theories have been suggested as potential frameworks for modelling biodiversity. Niche models assume that biological traits represent evolutionary adaptations and define individuals in terms of functional trade-offs. Neutral models assume that all individuals at a single trophic level are functionally equivalent on a per capita basis with respect to their birth, death, dispersal and speciation. The opinion of many researchers is that neutral and niche processes operate simultaneously to generate diversity without knowing how the unification of both models can be achieved. Recently, several theoretical papers have reported evidence on the evolutionary emergence of niche structures shaping the emergence of groups of similar species. In this way, an Emergent Group is defined as a set of species that have a similar functional niche owing to a convergent ecological strategy. Central to the Emergent Group concept are the assumptions of functional equivalence within and of functional divergence between Emergent Groups. Within an Emergent Group, species richness is subject to a zero-sum rule set by the balance between the rate of individual loss and of immigration. Between Emergent Groups, tradeoffs such as seed size/seedling competitivity, investment in reproductive system/investment in vegetative systems or competitive ability/predator invulnerability are cornerstones of the evolutionary divergence. Delineating Emergent Groups amounts to reaching a compromise between maximizing niche differentiation (i.e. maximizing differences in functional tradeoffs) between Emergent Groups and maximizing neutrality within Emergent Groups. Up to now, the Emergent Group concept has been mostly proposed by theoretical scientists but it should be tested by empirical ecologists. The way in which niche and neutral models could be combined provides a profitable opportunity for theoretical and empirical scientists to collaborate fruitfully.     

Epistasis can accelerate adaptive diversification in haploid asexual populations

A fundamental goal of the biological sciences is to determine processes that facilitate the evolution of diversity. These processes can be separated into ecological, physiological, developmental and genetic. An ecological process that facilitates diversification is frequency-dependent selection caused by competition. Models of frequency-dependent adaptive diversification have generally assumed a genetic basis of phenotype that is non-epistatic. Here, we present a model that indicates diversification is accelerated by an epistatic basis of phenotype in combination with a competition model that invokes frequency-dependent selection. Our model makes use of a genealogical model of epistasis and insights into the effects of balancing selection on the genealogical structure of a population to understand how epistasis can facilitate diversification. The finding that epistasis facilitates diversification may be informative with respect to empirical results that indicate an epistatic basis of phenotype in experimental bacterial populations that experienced adaptive diversification.     

Slow molecular evolution in an ancient asexual ostracod

Genetic variability of the non-marine ostracod species Darwinula stevensoni was estimated by sequencing part of the nuclear and the mitochondrial genome. As Darwinulidae are believed to be ancient asexuals, accumulation of mutations should have occurred, both between alleles within lineages and between lineages, during the millions of years of parthenogenetic reproduction. However, our sequence data show the opposite: no variability in the nuclear ITS1 region was observed within or among individuals of D. stevensoni, despite sampling a geographical range from Finland to South Africa. Lack of allelic divergence might be explained by concerted evolution of rDNA repeats. Homogeneity among individuals may be caused either by slow molecular evolution in ITS1 or by a recent selective sweep. Variability of mitochondrial cytochrome oxidase (COI) was similar to intraspecific levels in other invertebrates, thus weakening the latter hypothesis. Calibrating interspecific, genetic divergences among D. stevensoni and other Darwinulidae using their fossil record enabled us to estimate rates of molecular evolution. Both COI and ITS1 evolve half as fast, at most, in darwinulids as in other invertebrates, and molecular evolution has significantly slowed down in ITS1 of D. stevensoni relative to other darwinulids. A reduced ITS1 mutation rate might explain this inconsistency between nuclear and mitochondrial evolution in D. stevensoni.     

Adaptive evolution in a spatially structured asexual population

We study the process of adaptation in a spatially structured asexual haploid population. The model assumes a local competition for replication, where each organism interacts only with its nearest neighbors. We observe that the substitution rate of beneficial mutations is smaller for a spatially structured population than that seen for populations without structure. The difference between structured and unstructured populations increases as the adaptive mutation rate increases. Furthermore, the substitution rate decreases as the number of neighbors for local competition is reduced. We have also studied the impact of structure on the distribution of adaptive mutations that fix during adaptation.     

The evolution of stress-induced hypermutation in asexual populations

Numerous empirical studies show that stress of various kinds induces a state of hypermutation in bacteria via multiple mechanisms, but theoretical treatment of this intriguing phenomenon is lacking. We used deterministic and stochastic models to study the evolution of stress-induced hypermutation in infinite and finite-size populations of bacteria undergoing selection, mutation, and random genetic drift in constant environments and in changing ones. Our results suggest that if beneficial mutations occur, even rarely, then stress-induced hypermutation is advantageous for bacteria at both the individual and the population levels and that it is likely to evolve in populations of bacteria in a wide range of conditions because it is favored by selection. These results imply that mutations are not, as the current view holds, uniformly distributed in populations, but rather that mutations are more common in stressed individuals and populations. Because mutation is the raw material of evolution, these results have a profound impact on broad aspects of evolution and biology.     

Constraints on the evolution of asexual reproduction

Sexual reproduction is almost ubiquitous among multicellular organisms even though it entails severe fitness costs. To resolve this apparent paradox, an extensive body of research has been devoted to identifying the selective advantages of recombination that counteract these costs. Yet, how easy is it to make the transition to asexual reproduction once sexual reproduction has been established for a long time? The present review approaches this question by considering factors that impede the evolution of parthenogenesis in animals. Most importantly, eggs need a diploid chromosome set in most species in order to develop normally. Next, eggs may need to be activated by sperm, and sperm may also contribute centrioles and other paternal factors to the zygote. Depending on how diploidy is achieved mechanistically, further problems may arise in offspring that stem from 'inbreeding depression' or inappropriate sex determination systems. Finally, genomic imprinting is another well-known barrier to the evolution of asexuality in mammals. Studies on species with occasional, deficient parthenogenesis indicate that the relative importance of these constraints may vary widely. The intimate evolutionary relations between haplodiploidy and parthenogenesis as well as implications for the clade selection hypothesis of the maintenance of sexual reproduction are also discussed.     

The evolution of mutation rate in finite asexual populations

In this article, we model analytically the evolution of mutation rate in asexual organisms. Three selective forces are present. First, everything else being equal, individuals with higher mutation rate have a larger fitness, thanks to the energy and time saved by not replicating DNA accurately. Second, as a flip side, the genome of these individuals is replicated with errors that may negatively affect fitness. Third, and conversely, replication errors have a potential benefit if beneficial mutations are to be generated. Our model describes the fate of modifiers of mutation rate under the three forces and allows us to predict the long-term evolutionary trajectory of mutation rate. We obtain three major results. First, in asexuals, the needs for both adaptation and genome preservation are not evolutionary forces that can stabilize mutation rate at an intermediate optimum. When adaptation has a significant role, it primarily destabilizes mutation rate and yields the emergence of strong-effect mutators. Second, in contrast to what is usually believed, the appearance of modifiers with large mutation rate is more likely when the fitness cost of each deleterious mutation is weak, because the cost of replication errors is then paid after a delay. Third, in small populations, and even if adaptations are needed, mutation rate is always blocked at the minimum attainable level, because the rate of adaptation is too slow to play a significant role. Only populations whose size is above a critical mass see their mutation rate affected by the need for adaptation.     

Emergent and effective properties in ecology and evolution

Emergent properties are often discussed in arguments concerning relationships among different levels. However, the different definitions of emergent properties sometimes confuse the arguments about macro-level phenomena, since some authors regard emergent properties not only as observable global patterns but as properties that affect and cause change in ecological and evolutionary processes. Thus it is important to distinguish higher-level or larger-scale properties that can influence particular ecological and evolutionary processes from those that cannot. I call the former properties effective properties. I gave examples that show why the distinctions between effective and non-effective properties are important.

     

Adaptive evolution of asexual populations under Muller's ratchet

We study the population genetics of adaptation in nonequilibrium haploid asexual populations. We find that the accumulation of deleterious mutations, due to the operation of Muller's ratchet, can considerably reduce the rate of fixation of advantageous alleles. Such reduction can be approximated reasonably well by a reduction in the effective population size. In the absence of Muller's ratchet, a beneficial mutation can only become fixed if it creates the best possible genotype; if Muller's ratchet operates, however, mutations initially arising in a nonoptimal genotype can also become fixed in the population, since the loss of the least-loaded class implies that an initially nonoptimal background can become optimal. We show that, while the rate at which adaptive mutations become fixed is reduced, the rate of fixation of deleterious mutations due to the ratchet is not changed by the presence of beneficial mutations as long as the rate of their occurrence is low and the deleterious effects of mutations (s(d)) are higher than the beneficial effects (s(a)). When s(a) > s(d), the advantage of a beneficial mutation can outweigh the deleterious effects of associated mutations. Under these conditions, a beneficial allele can drag to fixation deleterious mutations initially associated with it at a higher rate than in the absence of advantageous alleles. We propose analytical approximations for the rates of accumulation of deleterious and beneficial mutations. Furthermore, when allowing for the possible occurrence of interference between beneficial alleles, we find that the presence of deleterious mutations of either very weak or very strong effect can marginally increase the rate of accumulation of beneficial mutations over that observed in the absence of such deleterious mutations.     

Microbial adaptive evolution

Bacterial species can adapt to significant changes in their environment by mutation followed by selection, a phenomenon known as “adaptive evolution.” With the development of bioinformatics and genetic engineering, research on adaptive evolution has progressed rapidly, as have applications of the process. In this review, we summarize various mechanisms of bacterial adaptive evolution, the technologies used for studying it, and successful applications of the method in research and industry. We particularly highlight the contributions of Dr. L. O. Ingram. Microbial adaptive evolution has significant impact on our society not only from its industrial applications, but also in the evolution, emergence, and control of various pathogens.     

Predicting adaptive evolution

Phylogenetic trees reconstruct past evolution and can provide evidence of past evolutionary pressure on genes and on individual codons. In addition to tracing past evolutionary events, molecular phylogenetics might also be used to predict future evolution. Our ability to verify adaptive hypotheses using phylogenetics has broad implications for vaccine design, genomics and structural biology.     

Fluctuation domains in adaptive evolution

We derive an expression for the variation between parallel trajectories in phenotypic evolution, extending the well known result that predicts the mean evolutionary path in adaptive dynamics or quantitative genetics. We show how this expression gives rise to the notion of fluctuation domains-parts of the fitness landscape where the rate of evolution is very predictable (due to fluctuation dissipation) and parts where it is highly variable (due to fluctuation enhancement). These fluctuation domains are determined by the curvature of the fitness landscape. Regions of the fitness landscape with positive curvature, such as adaptive valleys or branching points, experience enhancement. Regions with negative curvature, such as adaptive peaks, experience dissipation. We explore these dynamics in the ecological scenarios of implicit and explicit competition for a limiting resource.     

The speed of evolution and maintenance of variation in asexual populations

BACKGROUND: The rate at which beneficial mutations accumulate determines how fast asexual populations evolve, but this is only partially understood. Some recent clonal-interference models suggest that evolution in large asexual populations is limited because smaller beneficial mutations are outcompeted by larger beneficial mutations that occur in different lineages within the same population. This analysis assumes that the important mutations fix one at a time; it ignores multiple beneficial mutations that occur in the lineage of an earlier beneficial mutation, before the first mutation in the series can fix. We focus on the effects of such multiple mutations. RESULTS: Our analysis predicts that the variation in fitness maintained by a continuously evolving population increases as the logarithm of the population size and logarithm of the mutation rate and thus yields a similar logarithmic increase in the speed of evolution. To test these predictions, we evolved asexual budding yeast in glucose-limited media at a range of population sizes and mutation rates. CONCLUSIONS: We find that their evolution is dominated by the accumulation of multiple mutations of moderate effect. Our results agree with our theoretical predictions and are inconsistent with the one-by-one fixation of mutants assumed by recent clonal-interference analysis.     

Effects of selective neutrality on the evolution of molecular species

We introduce a model of evolution on a fitness landscape possessing a tunable degree of neutrality. The model allows us to study the general properties of molecular species undergoing neutral evolution. We find that a number of phenomena seen in RNA sequence-structure maps are present also in our general model. Examples are the occurrence of ''common'' structures that occupy a fraction of the genotype space which tends to unity as the length of the genotype increases, and the formation of percolating neutral networks that cover the genotype space in such a way that a member of such a network can be found within a small radius of any point in the space. We also describe a number of new phenomena that appear to be general properties of systems possessing selective neutrality. In particular, we show that the maximum fitness attained during the adaptive walk of a population evolving on such a fitness landscape increases with increasing degree of neutrality, and is directly related to the fitness of the most fit percolating network.     

Nearly neutrality and the evolution of codon usage bias in eukaryotic genomes

Here I show that the mean codon usage bias of a genome, and of the lowly expressed genes in a genome, is largely similar across eukaryotes ranging from unicellular protists to vertebrates. Conversely, this bias in housekeeping genes and in highly expressed genes has a remarkable inverse relationship with species generation time that varies by more than four orders of magnitude. The relevance of these results to the nearly neutral theory of molecular evolution is discussed.     

The effect of population bottlenecks on mutation rate evolution in asexual populations

In the absence of recombination, a mutator allele can spread through a population by hitchhiking with beneficial mutations that appear in its genetic background. Theoretical studies over the past decade have shown that the survival and fixation probability of beneficial mutations can be severely reduced by population size bottlenecks. Here, we use computational modelling and evolution experiments with the yeast S. cerevisiae to examine whether population bottlenecks can affect mutator dynamics in adapting asexual populations. In simulation, we show that population bottlenecks can inhibit mutator hitchhiking with beneficial mutations and are most effective at lower beneficial mutation supply rates. We then subjected experimental populations of yeast propagated at the same effective population size to three different bottleneck regimes and observed that the speed of mutator hitchhiking was significantly slower at smaller bottlenecks, consistent with our theoretical expectations. Our results, thus, suggest that bottlenecks can be an important factor in mutation rate evolution and can in certain circumstances act to stabilize or, at least, delay the progressive elevation of mutation rates in asexual populations. Additionally, our findings provide the first experimental support for the theoretically postulated effect of population bottlenecks on beneficial mutations and demonstrate the usefulness of studying mutator frequency dynamics for understanding the underlying dynamics of fitness‐affecting mutations.