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Host-parasite interactions in the form of infectious diseases are a topic of interest in both evolutionary biology and public health. Both fields have relied on mathematical models to predict and understand the dynamics and consequences of these interactions. Yet few models explicitly incorporate both epidemiological and coevolutionary dynamics, allowing for genetic variation in both hosts and parasites. By comparing a matching-alleles model of coevolution, a susceptible-infected-recovered-susceptible compartmental model from epidemiology, and a combined coevolutionary-epidemiology model we assess the effect of the coevolutionary feedback on the epidemiological dynamics and vice versa. We find that Red-Queen cycles are not robust in an epidemiological framework and that coevolutionary interactions can alter the conditions under which epidemic cycles arise. Incorporating both explicit epidemiology and genetic diversity may have important implications for the maintenance of sexual reproduction as well as disease management., (Copyright © 2017 Elsevier Inc. All rights reserved.)

Changes in genome copy number have occurred numerous times throughout the history of life, with profound evolutionary consequences. New experiments with budding yeast shed light on how frequently spontaneous genome doubling occurs within populations and the environmental conditions that favour cells with doubled genomes., (Copyright © 2018 Elsevier Ltd. All rights reserved.)

Genome-wide association studies are widely used to identify "disease genes" conferring resistance/susceptibility to infectious diseases. Using a combination of mathematical models and simulations, we demonstrate that genetic interactions between hosts and parasites [genotype-by-genotype (G × G) interactions] can drastically affect the results of these association scans and hamper our ability to detect genetic variation in susceptibility. When hosts and parasites coevolve, these G × G interactions often make genome-wide association studies unrepeatable over time or across host populations. Reanalyzing previously published data on Daphnia magna susceptibility to infection by Pasteuria ramosa , we identify genomic regions consistent with G × G interactions. We conclude by outlining possible avenues for designing more powerful and more repeatable association studies., (Copyright © 2018 by the Genetics Society of America.)

To date, research on the evolution of sex chromosomes has focused on sexually antagonistic selection among diploids, which has been shown to be a potent driver of the strata and reduced recombination that characterize many sex chromosomes. However, significant selection can also occur on haploid genotypes during less conspicuous life cycle stages, e.g. , competition among sperm/pollen or meiotic drive during gamete/spore production. These haploid selective processes are typically sex-specific, e.g. , gametic/gametophytic competition typically occurs among sperm/pollen, and meiotic drive typically occurs during either spermatogenesis or oogenesis. We use models to investigate whether sex-specific selection on haploids could drive the evolution of recombination suppression on the sex chromosomes, as has been demonstrated for sex-specific selection among diploids. A potential complication is that zygotic sex-ratios become biased when haploid selected loci become linked to the sex-determining region because the zygotic sex ratio is determined by the relative number and fitness of X- vs. Y-bearing sperm. Despite causing biased zygotic sex-ratios, we find that a period of sex-specific haploid selection generally favors recombination suppression on the sex chromosomes. Suppressed recombination is favored because it allows associations to build up between haploid-beneficial alleles and the sex that experiences haploid selection most often ( e.g. , pollen beneficial alleles become strongly associated with the male determining region, Y or Z). Haploid selected loci can favor recombination suppression even in the absence of selective differences between male and female diploids. Overall, we expand our view of the sex-specific life cycle stages that can drive sex chromosome evolution to include gametic competition and meiotic drive. Based on our models, sex chromosomes should become enriched for genes that experience haploid selection, as is expected for genes that experience sexually antagonistic selection. Thus, we generate a number of predictions that can be evaluated in emerging sex chromosome systems., (Copyright © 2017 by the Genetics Society of America.)

To persist in a changing world, populations must adapt. The ability to adapt is influenced by interactions with other species, such as predators. Recent experiments and theory suggest that selective pressures arising from predation may help prey adapt phenotypically to changing environments, but how this influences persistence remains unclear. In particular, it has not yet been shown whether predator-induced adaptation can outweigh predator-imposed reductions in population size, allowing prey to persist when they would otherwise go extinct. Here we examine if (and if so, how) predation can enhance the ability of prey to persist in a directionally changing environment. To do so, we extend a single-species quantitative-genetics framework that predicts rates of environmental change beyond which populations go extinct. While we assume predation decreases prey density, we find that predators can indeed help prey persist if they sufficiently increase prey adaptedness (decrease phenotypic lag). We show two ways this can occur: (1) the selective push, in which predators consume maladapted individuals and thus add selection that pushes the mean prey trait toward its optimum; and (2) the evolutionary hydra effect, when predation reduces prey density and thereby increases prey birthrate, allowing more selective events per unit time and effectively reducing generation time. We also discuss how our results apply more broadly to sources of mortality beyond predation.

Interspecific competition can strongly influence the evolutionary response of a species to a changing environment, impacting the chance that the species survives or goes extinct. Previous work has shown that when two species compete for a temporally shifting resource distribution, the species lagging behind the resource peak is the first to go extinct due to competitive exclusion. However, this work assumed symmetrically distributed resources and competition. Asymmetries can generate differences between species in population sizes, genetic variation and trait means. We show that asymmetric resource availability or competition can facilitate coexistence and even occasionally cause the leading species to go extinct first. Surprisingly, we also find cases where traits evolve in the opposite direction to the changing environment because of a 'vacuum of competitive release' created when the lagging species declines in number. Thus, the species exhibiting the slowest rate of trait evolution is not always the most likely to go extinct in a changing environment. Our results demonstrate that the extent to which species appear to be tracking environmental change and the extent to which they are preadapted to that change may not necessarily determine which species will be the winners and which will be the losers in a rapidly changing world., (© 2017 The Author(s).)

Sexual system is a key determinant of genetic variation and reproductive success, affecting evolution within populations and within clades. Much research in plants has focused on evolutionary transitions away from the most common state of hermaphroditism and toward the rare state of dioecy (separate sexes). Rather than transitions predominantly toward greater sexual differentiation, however, evolution may proceed in the direction of lesser sexual differentiation. We analyzed the macroevolutionary dynamics of sexual system in angiosperm genera that contain both dioecious and nondioecious species. Our phylogenetic analyses encompass a total of 2145 species from 40 genera. Overall, we found little evidence that rates of sexual system transitions are greater in any direction. Counting the number of inferred state changes revealed a mild prevalence of transitions away from hermaphroditism and away from dioecy, toward states of intermediate sexual differentiation. We identify genera in which future studies of sexual system evolution might be especially productive, and we discuss how integrating genetic or population-level studies of sexual system could improve the power of phylogenetic comparative analyses. Our work adds to the evidence that different selective pressures and constraints act in different groups, helping maintain the variety of sexual systems observed among plants., (© 2017 The Author(s). Evolution © 2017 The Society for the Study of Evolution.)

Current debates about the efficacy of no-take marine reserves (MR) in protecting large pelagic fish such as tuna and sharks have usually not considered the evolutionary dimension of this issue, which emerges because the propensity to swim away from a given place, like any other biological trait, will probably vary in a heritable fashion among individuals. Here, based on spatially explicit simulations, we investigated whether selection to remain in MRs to avoid higher fishing mortality can lead to the evolution of more philopatric fish. Our simulations, which covered a range of life histories among tuna species (skipjack tuna vs. Atlantic bluefin tuna) and shark species (great white sharks vs. spiny dogfish), suggested that MRs were most effective at maintaining viable population sizes when movement distances were lowest. Decreased movement rate evolved following the establishment of marine reserves, and this evolution occurred more rapidly with higher fishing pressure. Evolutionary reductions in movement rate led to increases in within-reserve population sizes over the course of the 50 years following MR establishment, although this varied among life histories, with skipjack responding fastest and great white sharks slowest. Our results suggest the evolution of decreased movement can augment the efficacy of marine reserves, especially for species, such as skipjack tuna, with relatively short generation times. Even when movement rates did not evolve substantially over 50 years (e.g., given long generation times or little heritable variation), marine reserves were an effective tool for the conservation of fish populations when mean movement rates were low or MRs were large.

Independently evolving populations may adapt to similar selection pressures via different genetic changes. The interactions between such changes, such as in a hybrid individual, can inform us about what course adaptation may follow and allow us to determine whether gene flow would be facilitated or hampered following secondary contact. We used Saccharomyces cerevisiae to measure the genetic interactions between first-step mutations that independently evolved in the same biosynthetic pathway following exposure to the fungicide nystatin. We found that genetic interactions are prevalent and predominantly negative, with the majority of mutations causing lower growth when combined in a double mutant than when alone as a single mutant (sign epistasis). The prevalence of sign epistasis is surprising given the small number of mutations tested and runs counter to expectations for mutations arising in a single biosynthetic pathway in the face of a simple selective pressure. Furthermore, in one third of pairwise interactions, the double mutant grew less well than either single mutant (reciprocal sign epistasis). The observation of reciprocal sign epistasis among these first adaptive mutations arising in the same genetic background indicates that partial postzygotic reproductive isolation could evolve rapidly between populations under similar selective pressures, even with only a single genetic change in each. The nature of the epistatic relationships was sensitive, however, to the level of drug stress in the assay conditions, as many double mutants became fitter than the single mutants at higher concentrations of nystatin. We discuss the implications of these results both for our understanding of epistatic interactions among beneficial mutations in the same biochemical pathway and for speciation., Competing Interests: The authors have declared that no competing interests exist.

Classical population genetic theory generally assumes either a fully haploid or fully diploid life cycle. However, many organisms exhibit more complex life cycles, with both free-living haploid and diploid stages. Here we ask what the probability of fixation is for selected alleles in organisms with haploid-diploid life cycles. We develop a genetic model that considers the population dynamics using both the Moran model and Wright-Fisher model. Applying a branching process approximation, we obtain an accurate fixation probability assuming that the population is large and the net effect of the mutation is beneficial. We also find the diffusion approximation for the fixation probability, which is accurate even in small populations and for deleterious alleles, as long as selection is weak. These fixation probabilities from branching process and diffusion approximations are similar when selection is weak for beneficial mutations that are not fully recessive. In many cases, particularly when one phase predominates, the fixation probability differs substantially for haploid-diploid organisms compared to either fully haploid or diploid species., (Copyright © 2017 by the Genetics Society of America.)

Measuring reproductive barriers between groups of organisms is an effective way to determine the traits and mechanisms that impede gene flow. However, to understand the ecological and evolutionary factors that drive speciation, it is important to distinguish between the barriers that arise early in the speciation process and those that arise after speciation is largely complete. In this article, we comprehensively test for reproductive isolation between recently diverged (<10,000 years bp) dune and nondune ecotypes of the prairie sunflower, Helianthus petiolaris. We find reproductive barriers acting at multiple stages of hybridization, including premating, postmating-prezygotic, and postzygotic barriers, despite the recent divergence. Barriers include extrinsic selection against immigrants and hybrids, a shift in pollinator assemblage, and postpollination assortative mating. Together, these data suggest that multiple barriers can be important for reducing gene flow in the earliest stages of speciation., (© 2016 The Author(s). Evolution © 2016 The Society for the Study of Evolution.)

In the absence of migration, species persistence depends on adaption to a changing environment, but whether and how adaptation to global change is altered by community diversity is not understood. Community diversity may prevent, enhance or alter how species adapt to changing conditions by influencing population sizes, genetic diversity and/or the fitness landscape experienced by focal species. We tested the impact of community diversity on adaptation by performing a reciprocal transplant experiment on grasses that evolved for 14 years under ambient and elevated CO2, in communities of low or high species richness. Using biomass as a fitness proxy, we find evidence for local adaptation to elevated CO2, but only for plants assayed in a community of similar diversity to the one experienced during the period of selection. Our results indicate that the biological community shapes the very nature of the fitness landscape within which species evolve in response to elevated CO2.

Few topics have intrigued biologists as much as the evolution of sex. Understanding why sex persists despite its costs requires not just rigorous theoretical study, but also empirical data on related fundamental issues, including the nature of genetic variance for fitness, patterns of genetic interactions, and the dynamics of adaptation. The increasing feasibility of examining genomes in an experimental context is now shedding new light on these problems. Using this approach, McDonald et al. recently demonstrated that sex uncouples beneficial and deleterious mutations, allowing selection to proceed more effectively with sex than without. Here we discuss the insights provided by this study, along with other recent empirical work, in the context of the major theoretical models for the evolution of sex., (© 2016 WILEY Periodicals, Inc.)

Species' life history traits, including maturation age, number of reproductive bouts, offspring size and number, reflect adaptations to diverse biotic and abiotic selection pressures. A striking example of divergent life histories is the evolution of either iteroparity (breeding multiple times) or semelparity (breed once and die). We analysed published data on salmonid fishes and found that semelparous species produce larger eggs, that egg size and number increase with salmonid body size among populations and species and that migratory behaviour and parity interact. We developed three hypotheses that might explain the patterns in our data and evaluated them in a stage-structured modelling framework accounting for different growth and survival scenarios. Our models predict the observation of small eggs in iteroparous species when egg size is costly to maternal survival or egg number is constrained. By exploring trait co-variation in salmonids, we generate new hypotheses for the evolution of trade-offs among life history traits., (© 2016 John Wiley & Sons Ltd/CNRS.)

In finite populations, mutation limitation and genetic drift can hinder evolutionary diversification. We consider the evolution of a quantitative trait in an asexual population whose size can vary and depends explicitly on the trait. Previous work showed that evolutionary branching is certain ("deterministic branching") above a threshold population size, but uncertain ("stochastic branching") below it. Using the stationary distribution of the population's trait variance, we identify three qualitatively different sub-domains of "stochastic branching" and illustrate our results using a model of social evolution. We find that in very small populations, branching will almost never be observed; in intermediate populations, branching is intermittent, arising and disappearing over time; in larger populations, finally, branching is expected to occur and persist for substantial periods of time. Our study provides a clearer picture of the ecological conditions that facilitate the appearance and persistence of novel evolutionary lineages in the face of genetic drift., (Copyright © 2015 Elsevier Inc. All rights reserved.)

Diploid organisms manipulate the extent to which their haploid gametes experience selection. Animals typically produce sperm with a diploid complement of most proteins and RNA, limiting selection on the haploid genotype. Plants, however, exhibit extensive expression in pollen, with actively transcribed haploid genomes. Here we analyze models that track the evolution of genes that modify the strength of haploid selection to predict when evolution intensifies and when it dampens the "selective arena" within which male gametes compete for fertilization. Considering deleterious mutations, evolution leads diploid mothers to strengthen selection among haploid sperm/pollen, because this reduces the mutation load inherited by their diploid offspring. If, however, selection acts in opposite directions in haploids and diploids ("ploidally antagonistic selection"), mothers evolve to reduce haploid selection to avoid selectively amplifying alleles harmful to their offspring. Consequently, with maternal control, selection in the haploid phase either is maximized or reaches an intermediate state, depending on the deleterious mutation rate relative to the extent of ploidally antagonistic selection. By contrast, evolution generally leads diploid fathers to mask mutations in their gametes to the maximum extent possible, whenever masking (e.g., through transcript sharing) increases the average fitness of a father's gametes. We discuss the implications of this maternal-paternal conflict over the extent of haploid selection and describe empirical studies needed to refine our understanding of haploid selection among seemingly diploid organisms.

Simple and ubiquitous gene interactions create rugged fitness landscapes composed of coadapted gene complexes separated by "valleys" of low fitness. Crossing such fitness valleys allows a population to escape suboptimal local fitness peaks to become better adapted. This is the premise of Sewall Wright's shifting balance process. Here we generalize the theory of fitness-valley crossing in the two-locus, bi-allelic case by allowing bias in parent-offspring transmission. This generalization extends the existing mathematical framework to genetic systems with segregation distortion and uniparental inheritance. Our results are also flexible enough to provide insight into shifts between alternate stable states in cultural systems with "transmission valleys". Using a semi-deterministic analysis and a stochastic diffusion approximation, we focus on the limiting step in valley crossing: the first appearance of the genotype on the new fitness peak whose lineage will eventually fix. We then apply our results to specific cases of segregation distortion, uniparental inheritance, and cultural transmission. Segregation distortion favouring mutant alleles facilitates crossing most when recombination and mutation are rare, i.e., scenarios where crossing is otherwise unlikely. Interactions with more mutable genes (e.g., uniparental inherited cytoplasmic elements) substantially reduce crossing times. Despite component traits being passed on poorly in the previous cultural background, small advantages in the transmission of a new combination of cultural traits can greatly facilitate a cultural transition. While peak shifts are unlikely under many of the common assumptions of population genetic theory, relaxing some of these assumptions can promote fitness-valley crossing., (Copyright © 2015 Elsevier Inc. All rights reserved.)

Chromosomal fusion plays a recurring role in the evolution of adaptations and reproductive isolation among species, yet little is known of the evolutionary drivers of chromosomal fusions. Because sex chromosomes (X and Y in male heterogametic systems, Z and W in female heterogametic systems) differ in their selective, mutational, and demographic environments, those differences provide a unique opportunity to dissect the evolutionary forces that drive chromosomal fusions. We estimate the rate at which fusions between sex chromosomes and autosomes become established across the phylogenies of both fishes and squamate reptiles. Both the incidence among extant species and the establishment rate of Y-autosome fusions is much higher than for X-autosome, Z-autosome, or W-autosome fusions. Using population genetic models, we show that this pattern cannot be reconciled with many standard explanations for the spread of fusions. In particular, direct selection acting on fusions or sexually antagonistic selection cannot, on their own, account for the predominance of Y-autosome fusions. The most plausible explanation for the observed data seems to be (a) that fusions are slightly deleterious, and (b) that the mutation rate is male-biased or the reproductive sex ratio is female-biased. We identify other combinations of evolutionary forces that might in principle account for the data although they appear less likely. Our results shed light on the processes that drive structural changes throughout the genome.

Evolutionary biologists have often assumed that ecological generalism comes at the expense of less intense exploitation of specific resources and that this trade-off will promote the evolution of ecologically specialized daughter species. Using a phylogenetic comparative approach with butterflies as a model system, we test hypotheses that incorporate changes in niche breadth and location into explanations of the taxonomic diversification of insect herbivores. Specifically, we compare the oscillation hypothesis, where speciation is driven by host-plant generalists giving rise to specialist daughter species, to the musical chairs hypothesis, where speciation is driven by host-plant switching, without changes in niche breadth. Contrary to the predictions of the oscillation hypothesis, we recover a negative relationship between host-plant breadth and diversification rate and find that changes in host breadth are seldom coupled to speciation events. By contrast, we present evidence for a positive relationship between rates of host switching and butterfly diversification, consonant with the musical chairs hypothesis. These results suggest that the costs of trophic generalism in plant-feeding insects may have been overvalued and that transitions from generalists to ecological specialists may not be an important driver of speciation in general., (© 2014 The Author(s) Published by the Royal Society. All rights reserved.)

Females vary in the size of offspring that they produce, often in a manner that depends on maternal age or stage. This is puzzling, given that offspring size is predicted to evolve to a single optimal value where the gain in fitness from being larger exactly offsets the fitness lost to the mother by producing fewer offspring. We used a stage-structured life-history model to determine the optimal offspring size for females in different stages. We found that optimal offspring size does not vary with maternal stage when offspring fitness depends only on its size and not on the stage of the mother. This negative result holds even with density dependence, when larger offspring compete better. However, a trade-off between offspring size and maternal survival affects the optimal offspring size. The future reproductive value of the female, coupled with the costs and benefits of offspring investment, drives the evolution of stage-dependent offspring size. If producing larger offspring is riskier for mothers, females produce smaller offspring when their reproductive value in the next time step is large relative to current reproductive prospects. These analyses provide a novel framework for understanding why offspring size varies in age- and stage-structured populations.

Environmental change, if severe, can drive a population extinct unless the population succeeds in adapting to the new conditions. How likely is a population to win the race between population decline and adaptive evolution? Assuming that environmental degradation progresses across a habitat, we analyze the impact of several ecological factors on the probability of evolutionary rescue. Specifically, we study the influence of population structure and density-dependent competition as well as the speed and severity of environmental change. We also determine the relative contribution of standing genetic variation and new mutations to evolutionary rescue. To describe population structure, we use a generalized island model, where islands are affected by environmental deterioration one after the other. Our analysis is based on the mathematical theory of time-inhomogeneous branching processes and complemented by computer simulations. We find that in the interplay of various, partially antagonistic effects, the probability of evolutionary rescue can show nontrivial and unexpected dependence on ecological characteristics. In particular, we generally observe a nonmonotonic dependence on the migration rate between islands. Counterintuitively, under some circumstances, evolutionary rescue can occur more readily in the face of harsher environmental shifts, because of the reduced competition experienced by mutant individuals. Similarly, rescue sometimes occurs more readily when the entire habitat degrades rapidly, rather than progressively over time, particularly when migration is high and competition strong.

Dispersal moves individuals from patches where their immediate ancestors were successful to sites where their genotypes are untested. As a result, dispersal generally reduces fitness, a phenomenon known as "migration load." The strength of migration load depends on the pattern of dispersal and can be dramatically lessened or reversed when individuals move preferentially toward patches conferring higher fitness. Evolutionary ecologists have long modeled nonrandom dispersal, focusing primarily on its effects on population density over space, the maintenance of genetic variation, and reproductive isolation. Here, we build upon previous work by calculating how the extent of local adaptation and the migration load are affected when individuals differ in their dispersal rate in a genotype-dependent manner that alters their match to their environment. Examining a one-locus, two-patch model, we show that local adaptation occurs through a combination of natural selection and adaptive dispersal. For a substantial portion of parameter space, adaptive dispersal can be the predominant force generating local adaptation. Furthermore, genetic load may be largely averted with adaptive dispersal whenever individuals move before selective deaths occur. Thus, to understand the mechanisms driving local adaptation, biologists must account for the extent and nature of nonrandom, genotype-dependent dispersal, and the potential for adaptation via spatial sorting of genotypes.

Pleiotropy is the property of genes affecting multiple functions or characters of an organism. Genes vary widely in their degree of pleiotropy, but this variation is often considered a by-product of their evolutionary history. We present a functional theory of how pleiotropy may itself evolve. We consider genes that contribute to two functions, where contributing more to one function detracts from allocation to the second function. We show that whether genes become pleiotropic or specialize on a single function depends on the nature of trade-offs as gene activities contribute to different traits and on how the functionality of these traits affects fitness. In general, when a gene product can perform well at two functions, it evolves to do so, but not when pleiotropy would greatly disrupt each function. Consequently, reduced pleiotropy should often evolve, with genes specializing on the trait that is currently more important to fitness. Even when pleiotropy does evolve, not all genes are expected to become equally pleiotropic; genes with higher levels of expression are more likely to evolve greater pleiotropy. For the case of gene duplicates, we find that perfect subfunctionalization evolves only under stringent conditions. More often, duplicates are expected to maintain a certain degree of functional redundancy, with the gene contributing more to trait functionality evolving the highest degree of pleiotropy. Gene product interactions can facilitate subfunctionalization, but whether they do so depends on the curvature of the fitness surface. Finally, we find that stochastic gene expression favors pleiotropy by selecting for robustness in fitness components.

Although there is no known general explanation as to why sexual populations resist asexual invasion, previous work has shown that sexuals can outcompete asexuals in structured populations. However, it is currently unknown whether costly sex can be maintained with the weak structure that is commonly observed in nature. We investigate the conditions under which obligate sexuals resist asexual invasion in structured populations subject to recurrent mutation. We determine the level of population structure needed to disfavor asexuals, as calculated using the average F(st) between all pairs of demes. We show that the critical F(st) needed to maintain sex decreases as the population size increases, and approaches modest levels as observed in many natural populations. Sex is maintained with lower F(st) if there are both advantageous and deleterious mutation, if mutation rates are sufficiently high, and if deleterious mutants have intermediate selective strengths, which maximizes the effect of Muller's ratchet. Additionally, the critical F(st) needed to maintain sex is lower when there are a large number of subpopulations. Lower F(st) values are needed to maintain sex when demes vary substantially in their pairwise distances (e.g., when arrayed along one dimension), although this effect is often modest, especially if some long-distance dispersal is present., (© 2012 The Author(s). Evolution© 2012 The Society for the Study of Evolution.)

Beneficial mutations are required for adaptation to novel environments, yet the range of mutational pathways that are available to a population has been poorly characterized, particularly in eukaryotes. We assessed the genetic changes of the first mutations acquired during adaptation to a novel environment (exposure to the fungicide, nystatin) in 35 haploid lines of Saccharomyces cerevisiae. Through whole-genome resequencing we found that the genomic scope for adaptation was narrow; all adapted lines acquired a mutation in one of four late-acting genes in the ergosterol biosynthesis pathway, with very few other mutations found. Lines that acquired different ergosterol mutations in the same gene exhibited very similar tolerance to nystatin. All lines were found to have a cost relative to wild type in an unstressful environment; the level of this cost was also strongly correlated with the ergosterol gene bearing the mutation. Interestingly, we uncovered both positive and negative effects on tolerance to other harsh environments for mutations in the different ergosterol genes, indicating that these beneficial mutations have effects that differ in sign among environmental challenges. These results demonstrate that although the genomic target was narrow, different adaptive mutations can lead populations down different evolutionary pathways, with respect to their ability to tolerate (or succumb to) other environmental challenges.

Variation in diversification rates is often studied by investigating traits related to species' ecology and life history. Often, however, it is unknown whether these traits evolve gradually or in punctuated bursts during speciation. Using phylogenetic data and species' present-day trait information, we present a novel approach to assessing the mode of character change while accounting for trait-dependent speciation and extinction. Our model, "Binary-State Speciation and Extinction-node enhanced state shift" (BiSSE-ness), estimates both the rate of change occurring along lineages and the probability of change occurring during speciation, as well as independent speciation and extinction rates for each character state. Using simulations, we found that BiSSE-ness is able to distinguish along-lineage and speciational change and accurately estimate the parameters associated with character change and diversification rates. We applied BiSSE-ness to an empirical primate data set and found evidence for along-lineage changes in primate mating systems and social behaviors, whereas shifts in habitat were associated with speciation. In cases where trait changes may be linked to the speciation process itself (e.g., niche-related traits), BiSSE-ness provides a suitable framework with which to simultaneously address questions regarding species diversification and character change.

Empirical data indicate that sexual preferences are critical for maintaining species boundaries, yet theoretical work has suggested that, on their own, they can have only a minimal role in maintaining biodiversity. This is because long-term coexistence within overlapping ranges is thought to be unlikely in the absence of ecological differentiation. Here we challenge this widely held view by generalizing a standard model of sexual selection to include two ubiquitous features of populations with sexual selection: spatial variation in local carrying capacity, and mate-search costs in females. We show that, when these two features are combined, sexual preferences can single-handedly maintain coexistence, even when spatial variation in local carrying capacity is so slight that it might go unnoticed empirically. This theoretical study demonstrates that sexual selection alone can promote the long-term coexistence of ecologically equivalent species with overlapping ranges, and it thus provides a novel explanation for the maintenance of species diversity.

Levels of parasitism are continuously distributed in nature. Models of host-parasite coevolution, however, typically assume that species can be easily characterized as either parasitic or non-parasitic. Consequently, it is poorly understood which factors influence the evolution of parasitism itself. We investigate how ploidy level and the genetic mechanisms underlying infection influence evolution along the continuum of parasitism levels. In order for parasitism to evolve, selective benefits to the successful invasion of hosts must outweigh the losses when encountering resistant hosts. However, we find that exactly where this threshold occurs depends not only on the strength of selection, but also on the genetic model of interaction, the ploidy level in each species, and the nature of the costs to virulence and resistance. With computer simulations, we are able to incorporate more realistic dynamics at the loci underlying species interactions and to extend our analyses in a number of directions, including finite population sizes, multiple alleles and different generation times., (This journal is © 2011 The Royal Society)

Rate heterogeneity within groups of organisms is known to exist even when closely related taxa are examined. A wide variety of phylogenetic and dating methods have been developed that aim either to test for the existence of rate variation or to correct for its bias. However, none of the existing methods track the evolution of features that account for observed rate heterogeneity. Here, we present a likelihood model that assumes that rate variation is caused, in part, by species' intrinsic characteristics, such as a particular life-history trait, morphological feature, or habitat association. The model combines models of sequence and character state evolution such that rates of sequence change depend on the character state of a lineage at each point in time. We test, using simulations, the power and accuracy of the model to determine whether rates of molecular evolution depend on a particular character state and demonstrate its utility using an empirical example with halophilic and freshwater daphniids.

Although the evolution of recombination is still a major problem in evolutionary genetics, recent theoretical studies have shown that recombination can evolve by breaking down interference ("Hill-Robertson effects") among multiple loci. This leads to selection on a recombination modifier in a population subject to recurrent deleterious mutation. Here, we use computer simulations to investigate the evolution of a recombination modifier under three different scenarios of recurrent mutation in a finite population: (1) mutations are deleterious only, (2) mutations are advantageous only, and (3) there is a mixture of deleterious and advantageous mutations. We also investigate how linkage disequilibrium, the strength of selection acting on a modifier, and effective population size change under the different scenarios. We observe that adding even a small number of advantageous mutations increases the fixation rate of modifiers that increase recombination, especially if the effects of deleterious mutations are weak. However, the strength of selection on a modifier is less than the summed strengths had there been deleterious mutations only and advantageous mutations only.

Genomes vary dramatically in size and in content. This variation is driven in part by numerous polyploidization events that have happened over the course of eukaryotic evolution. Experimental evolution studies, primarily using the yeast Saccharomyces cerevisiae, provide insights into the immediate fitness effects of ploidy mutations, the ability of organisms of different ploidy levels to mask deleterious mutations, the impact of ploidy on rates of adaptation, and the relative roles of selection versus drift in shaping ploidy evolution. We review these experimental evolution studies and present new data on differences in maximal growth rate for cells of different ploidy levels.

A long-standing goal in evolutionary biology is to identify the conditions that promote the evolution of reproductive isolation and speciation. The factors promoting sympatric speciation have been of particular interest, both because it is notoriously difficult to prove empirically and because theoretical models have generated conflicting results, depending on the assumptions made. Here, we analyze the conditions under which selection favors the evolution of assortative mating, thereby reducing gene flow between sympatric groups, using a general model of selection, which allows fitness to be frequency dependent. Our analytical results are based on a two-locus diploid model, with one locus altering the trait under selection and the other locus controlling the strength of assortment (a "one-allele" model). Examining both equilibrium and nonequilibrium scenarios, we demonstrate that whenever heterozygotes are less fit, on average, than homozygotes at the trait locus, indirect selection for assortative mating is generated. While costs of assortative mating hinder the evolution of reproductive isolation, they do not prevent it unless they are sufficiently great. Assortative mating that arises because individuals mate within groups (formed in time or space) is most conducive to the evolution of complete assortative mating from random mating. Assortative mating based on female preferences is more restrictive, because the resulting sexual selection can lead to loss of the trait polymorphism and cause the relative fitness of heterozygotes to rise above homozygotes, eliminating the force favoring assortment. When assortative mating is already prevalent, however, sexual selection can itself cause low heterozygous fitness, promoting the evolution of complete reproductive isolation (akin to "reinforcement") regardless of the form of natural selection.

Large-scale transitions in genome size from tetraploid to diploid were observed during a previous 1800-generation evolution experiment in Saccharomyces cerevisiae. Whether the transitions occurred via a one-step process (tetraploid to diploid) or through multiple steps (through ploidy intermediates) remained unclear. To provide insight into the mechanism involved, we investigated whether triploid-sized cells sampled from the previous experiment could also undergo ploidy loss. A batch culture experiment was conducted for approximately 200 generations, starting from four triploid-sized colonies and one contemporaneous tetraploid-sized colony. Ploidy reduction towards diploidy was observed in both triploid and tetraploid lines. Comparative genomic hybridization indicated the presence of aneuploidy in both the founder and the evolved colonies. The specific aneuploidies involved suggest that chromosome loss was not haphazard but that nearly full sets of chromosomes were lost at once, with some additional chromosome mis-segregation events. These results suggest the existence of a mitotic mechanism allowing the elimination of an entire set of chromosomes in S. cerevisiae, thereby reducing the ploidy level.

Facultatively sexual organisms often engage in sex more often when in poor condition. We show that such condition-dependent sex carries evolutionary advantages and can explain the evolution of sexual reproduction even when sex entails high costs. Specifically, we show that alleles promoting individuals of low fitness to have sex more often than individuals of high fitness spread through a population. Such alleles are more likely to segregate out of bad genetic backgrounds and onto good genetic backgrounds, where they tend to remain. This "abandon-ship" mechanism provides a plausible model for the evolution and maintenance of facultative sex.

The ubiquity of sexual reproduction despite its cost has lead to an extensive body of research on the evolution and maintenance of sexual reproduction. Previous work has suggested that sexual reproduction can substantially speed up the rate of adaptation in diploid populations, because sexual populations are able to produce the fittest homozygous genotype by segregation and mating of heterozygous individuals. In contrast, asexual populations must wait for two rare mutational events, one producing a heterozygous carrier and the second converting a heterozygous to a homozygous carrier, before a beneficial mutation can become fixed. By avoiding this additional waiting time, it was shown that the benefits of segregation could overcome a twofold cost of sex. This previous result ignores mitotic recombination (MR), however. Here, we show that MR significantly hastens the spread of beneficial mutations in asexual populations. Indeed, given empirical data on MR, we find that adaptation in asexual populations proceeds as fast as that in sexual populations, especially when beneficial alleles are partially recessive. We conclude that asexual populations can gain most of the benefit of segregation through MR while avoiding the costs associated with sexual reproduction.

Despite it being the darling of fungal genomics, we know little about either the ecology or reproductive biology of the budding yeast, Saccharomyces cerevisiae, in nature. A recent study by Ruderfer et al. estimated that the ancestors of three S. cerevisiae genomes outcrossed approximately once every 50,000 generations, confirming the view that outcrossing is infrequent in natural populations of S. cerevisiae. This study also inferred the genomic positions of past recombination events. By comparing past recombination events with present-day recombination rates, this study lays the groundwork for determining whether recombination has improved the long-term survival of descendant lineages by bringing together favorable alleles, a longstanding question in evolutionary genetics.

Evolutionary biologists have identified several factors that could explain the widespread phenomena of sex and recombination. One hypothesis is that host-parasite interactions favor sex and recombination because they favor the production of rare genotypes. A problem with many of the early models of this so-called Red Queen hypothesis is that several factors are acting together: directional selection, fluctuating epistasis, and drift. It is thus difficult to identify what exactly is selecting for sex in these models. Is one factor more important than the others or is it the synergistic action of these different factors that really matters? Here we focus on the analysis of a simple model with a single mechanism that might select for sex: fluctuating epistasis. We first analyze the evolution of sex and recombination when the temporal fluctuations are driven by the abiotic environment. We then analyze the evolution of sex and recombination in a two-species coevolutionary model, where directional selection is absent (allele frequencies remain fixed) and temporal variation in epistasis is induced by coevolution with the antagonist species. In both cases we contrast situations with weak and strong selection and derive the evolutionarily stable (ES) recombination rate. The ES recombination rate is most sensitive to the period of the cycles, which in turn depends on the strength of epistasis. In particular, more virulent parasites cause more rapid cycles and consequently increase the ES recombination rate of the host. Although the ES strategy is maximized at an intermediate period, some recombination is favored even when fluctuations are very slow. By contrast, the amplitude of the cycles has no effect on the ES level of sex and recombination, unless sex and recombination are costly, in which case higher-amplitude cycles allow the evolution of higher rates of sex and recombination. In the coevolutionary model, the amount of recombination in the interacting species also has a large effect on the ES, with evolution favoring higher rates of sex and recombination than in the interacting species. In general, the ES recombination rate is less than or equal to the recombination rate that would maximize mean fitness. We also discuss the effect of migration when sex and recombination evolve in a metapopulation. We find that intermediate parasite migration rates maximize the degree of local adaptation of the parasite and lead to a higher ES recombination rate in the host.

In facultatively sexual species, lineages that reproduce asexually for a period of time can accumulate mutations that reduce their ability to undergo sexual reproduction when sex is favorable. We propagated Saccharomyces cerevisiae asexually for approximately 800 generations, after which we measured the change in sexual fitness, measured as the proportion of asci observed in sporulation medium. The sporulation rate in cultures propagated asexually at small population size declined by 8%, on average, over this time period, indicating that the majority of mutations that affect sporulation rate are deleterious. Interestingly, the sporulation rate in cultures propagated asexually at large population size improved by 11%, on average, indicating that selection on asexual function effectively eliminated most of the mutations deleterious to sporulation ability. These results suggest that pleiotropy between mutations' effects on asexual fitness and sexual fitness was predominantly positive, at least for the mutations accumulated in this experimental evolution study. A positive correlation between growth rate and sporulation rate among lines also provided evidence for positive pleiotropy. These results demonstrate that, at least under certain circumstances, selection acting on asexual fitness can help to maintain sexual function.

Sex and recombination are widespread, but explaining these phenomena has been one of the most difficult problems in evolutionary biology. Recombination is advantageous when different individuals in a population carry different advantageous alleles. By bringing together advantageous alleles onto the same chromosome, recombination speeds up the process of adaptation and opposes the fixation of harmful mutations by means of Muller's ratchet. Nevertheless, adaptive substitutions favour sex and recombination only if the rate of adaptive mutation is high, and Muller's ratchet operates only in small or asexual populations. Here, by tracking the fate of modifier alleles that alter the frequency of sex and recombination, we show that background selection against deleterious mutant alleles provides a stochastic advantage to sex and recombination that increases with population size. The advantage arises because, with low levels of recombination, selection at other loci severely reduces the effective population size and genetic variance in fitness at a focal locus (the Hill-Robertson effect), making a population less able to respond to selection and to rid itself of deleterious mutations. Sex and recombination reveal the hidden genetic variance in fitness by combining chromosomes of intermediate fitness to create chromosomes that are relatively free of (or are loaded with) deleterious mutations. This increase in genetic variance within finite populations improves the response to selection and generates a substantial advantage to sex and recombination that is fairly insensitive to the form of epistatic interactions between deleterious alleles. The mechanism supported by our results offers a robust and broadly applicable explanation for the evolutionary advantage of recombination and can explain the spread of costly sex.

Whether recombination decelerates or accelerates a population's response to selection depends, at least in part, on how fitness-determining loci interact. Realistically, all genomes likely contain fitness interactions both with positive and with negative epistasis. Therefore, it is crucial to determine the conditions under which the potential beneficial effects of recombination with negative epistasis prevail over the detrimental effects of recombination with positive epistasis. Here, we examine the simultaneous effects of diverse epistatic interactions with different strengths and signs in a simplified model system with independent pairs of interacting loci and selection acting only on the haploid phase. We find that the average form of epistasis does not predict the average amount of linkage disequilibrium generated or the impact on a recombination modifier when compared to results using the entire distribution of epistatic effects and associated single-mutant effects. Moreover, we show that epistatic interactions of a given strength can produce very different effects, having the greatest impact when selection is weak. In summary, we observe that the evolution of recombination at mutation-selection balance might be driven by a small number of interactions with weak selection rather than by the average epistasis of all interactions. We illustrate this effect with an analysis of published data of Saccharomyces cerevisiae. Thus to draw conclusions on the evolution of recombination from experimental data, it is necessary to consider the distribution of epistatic interactions together with the associated selection coefficients.

In finite populations, linkage disequilibria generated by the interaction of drift and directional selection (Hill-Robertson effect) can select for sex and recombination, even in the absence of epistasis. Previous models of this process predict very little advantage to recombination in large panmictic populations. In this article we demonstrate that substantial levels of linkage disequilibria can accumulate by drift in the presence of selection in populations of any size, provided that the population is subdivided. We quantify (i) the linkage disequilibrium produced by the interaction of drift and selection during the selective sweep of beneficial alleles at two loci in a subdivided population and (ii) the selection for recombination generated by these disequilibria. We show that, in a population subdivided into n demes of large size N, both the disequilibrium and the selection for recombination are equivalent to that expected in a single population of a size intermediate between the size of each deme (N) and the total size (nN), depending on the rate of migration among demes, m. We also show by simulations that, with small demes, the selection for recombination is stronger than both that expected in an unstructured population (m = 1 - 1/n) and that expected in a set of isolated demes (m = 0). Indeed, migration maintains polymorphisms that would otherwise be lost rapidly from small demes, while population structure maintains enough local stochasticity to generate linkage disequilibria. These effects are also strong enough to overcome the twofold cost of sex under strong selection when sex is initially rare. Overall, our results show that the stochastic theories of the evolution of sex apply to a much broader range of conditions than previously expected.

Sexual selection is a potent evolutionary force. However, very few models have considered the evolution of female preferences for traits expressed in both sexes. Here we explore how female preferences coevolve with sexually antagonistic traits, which involve alleles that are beneficial to one sex but harmful to the other. We show that with a sexually antagonistic trait on the X chromosome (males XY, females XX), females evolve to prefer mates carrying alleles beneficial to daughters. In contrast, with a Z-linked trait (males ZZ, females ZW), females more often evolve mating preferences for mates carrying alleles beneficial to sons (that is, flashy displays).

In finite populations subject to selection, genetic drift generates negative linkage disequilibrium, on average, even if selection acts independently (i.e., multiplicatively) upon all loci. Negative disequilibrium reduces the variance in fitness and hence, by Fisher's (1930) fundamental theorem, slows the rate of increase in mean fitness. Modifiers that increase recombination eliminate the negative disequilibria that impede selection and consequently increase in frequency by "hitchhiking." Thus, stochastic fluctuations in linkage disequilibrium in finite populations favor the evolution of increased rates of recombination, even in the absence of epistatic interactions among loci and even when disequilibrium is initially absent. The method developed within this article allows us to quantify the strength of selection acting on a modifier allele that increases recombination in a finite population. The analysis indicates that stochastically generated linkage disequilibria do select for increased recombination, a result that is confirmed by Monte Carlo simulations. Selection for a modifier that increases recombination is highest when linkage among loci is tight, when beneficial alleles rise from low to high frequency, and when the population size is small.

Pleiotropy is one of the most commonly observed attributes of genes. Yet the extent and influence of pleiotropy have been underexplored in population genetics models. In this paper, I quantify the extent to which pleiotropy inhibits the spread of alleles in response to directional selection on a focal trait. Under the assumption that pleiotropic effects are extensive and deleterious, the fraction of alleles that are beneficial overall is severely limited by pleiotropy and rises nearly linearly with the strength of directional selection on the focal trait. Over a broad class of distribution of pleiotropic effects, the mean selective effect of those alleles that are beneficial overall is halved, on average, by pleiotropy. The fraction of new mutant alleles that are beneficial overall and that succeed in fixing within a population is even more severely limited when directional selection is weak, but it rises quadratically with the strength of directional selection. Finally, the mean selective effect of mutant alleles that are beneficial and succeed in fixing is reduced by one-third, on average, by pleiotropy. These results help to shape our understanding of the evolutionary inertia caused by pleiotropy.

In diploids, sexual reproduction promotes both the segregation of alleles at the same locus and the recombination of alleles at different loci. This article is the first to investigate the possibility that sex might have evolved and been maintained to promote segregation, using a model that incorporates both a general selection regime and modifier alleles that alter an individual's allocation to sexual vs. asexual reproduction. The fate of different modifier alleles was found to depend strongly on the strength of selection at fitness loci and on the presence of inbreeding among individuals undergoing sexual reproduction. When selection is weak and mating occurs randomly among sexually produced gametes, reductions in the occurrence of sex are favored, but the genome-wide strength of selection is extremely small. In contrast, when selection is weak and some inbreeding occurs among gametes, increased allocation to sexual reproduction is expected as long as deleterious mutations are partially recessive and/or beneficial mutations are partially dominant. Under strong selection, the conditions under which increased allocation to sex evolves are reversed. Because deleterious mutations are typically considered to be partially recessive and weakly selected and because most populations exhibit some degree of inbreeding, this model predicts that higher frequencies of sex would evolve and be maintained as a consequence of the effects of segregation. Even with low levels of inbreeding, selection is stronger on a modifier that promotes segregation than on a modifier that promotes recombination, suggesting that the benefits of segregation are more likely than the benefits of recombination to have driven the evolution of sexual reproduction in diploids.

The segregation of alleles disrupts genetic associations at overdominant loci, causing a sexual population to experience a lower mean fitness compared to an asexual population. To investigate whether circumstances promoting increased sex exist within a population with heterozygote advantage, a model is constructed that monitors the frequency of alleles at a modifier locus that changes the relative allocation to sexual and asexual reproduction. The frequency of these modifier alleles changes over time as a correlated response to the dynamics at a fitness locus under overdominant selection. Increased sex can be favored in partially sexual populations that inbreed to some extent. This surprising finding results from the fact that inbred populations have an excess of homozygous individuals, for whom sex is always favorable. The conditions promoting increased levels of sex depend on the selection pressure against the homozygotes, the extent of sex and inbreeding in the population, and the dominance of the invading modifier allele.

Genetic variation in fitness is the fundamental prerequisite for adaptive evolutionary change. If there is no variation in survival and reproduction or if this variation has no genetic basis, then the composition of a population will not evolve over time. Consequently, the factors influencing genetic variation in fitness have received close attention from evolutionary biologists. One key factor is the mode of reproduction. Indeed, it has long been thought that sex enhances fitness variation and that this explains the ubiquity of sexual reproduction among eukaryotes. Nevertheless, theoretical studies have demonstrated that sex need not always increase genetic variation in fitness. In particular, if fitness interactions among beneficial alleles (epistasis) are positive, sex can reduce genetic variance in fitness. Empirical data have been sorely needed to settle the issue of whether sex does enhance fitness variation. A recent flurry of studies[1-4] has demonstrated that sex and recombination do dramatically increase genetic variation in fitness and consequently the rate of adaptive evolution. Interpreted in light of evolutionary theory, these studies rule out positive in these experiments epistasis as a major source of genetic associations. Further studies are needed, however, to tease apart other possible sources., (Copyright 2003 Wiley Periodicals, Inc.)

An unusually high proportion of proteins encoded in Chlamydia genomes are most similar to plant proteins, leading to proposals that a Chlamydia ancestor obtained genes from a plant or plant-like host organism by horizontal gene transfer. However, during an analysis of bacterial-eukaryotic protein similarities, we found that the vast majority of plant-like sequences in Chlamydia are most similar to plant proteins that are targeted to the chloroplast, an organelle derived from a cyanobacterium. We present further evidence suggesting that plant-like genes in Chlamydia, and other Chlamydiaceae, are likely a reflection of an unappreciated evolutionary relationship between the Chlamydiaceae and the cyanobacteria-chloroplast lineage. Further analyses of bacterial and eukaryotic genomes indicates the importance of evaluating organellar ancestry of eukaryotic proteins when identifying bacteria-eukaryote homologs or horizontal gene transfer and supports the proposal that Chlamydiaceae, which are obligate intracellular bacterial pathogens of animals, are not likely exchanging DNA with their hosts.