The joint evolution of lifespan and self‐fertilization

In Angiosperms, there exists a strong association between mating system and lifespan. Most self‐fertilizing species are short‐lived, and most predominant or obligate outcrossers are long‐lived. This association is generally explained by the influence of lifespan on the evolution of the mating system, considering lifespan as fixed. Yet, lifespan can itself evolve, and the mating system may as well influence the evolution of lifespan, as is suggested by joint evolutionary shifts of lifespan and mating system between sister species. In this paper, we build modifier models to study the joint evolution of self‐fertilization and lifespan, including both juvenile and adult inbreeding depression. We show that provided that inbreeding depression affects adult survival, self‐fertilization is expected to promote evolution towards shorter lifespan, and that the range of conditions under which selfing can evolve rapidly shrinks as lifespan increases. We study the effects of inbreeding depression affecting various steps in the life cycle and discuss how extrinsic mortality conditions are expected to affect evolutionary associations. In particular, we show that selfers may sometimes remain short‐lived even in a very stable habitat, as a strategy to avoid the deleterious effects of inbreeding.     

The contribution of the mitochondrial genome to sex‐specific fitness variance

Maternal inheritance of mitochondrial DNA (mtDNA) facilitates the evolutionary accumulation of mutations with sex‐biased fitness effects. Whereas maternal inheritance closely aligns mtDNA evolution with natural selection in females, it makes it indifferent to evolutionary changes that exclusively benefit males. The constrained response of mtDNA to selection in males can lead to asymmetries in the relative contributions of mitochondrial genes to female versus male fitness variation. Here, we examine the impact of genetic drift and the distribution of fitness effects (DFE) among mutations—including the correlation of mutant fitness effects between the sexes—on mitochondrial genetic variation for fitness. We show how drift, genetic correlations, and skewness of the DFE determine the relative contributions of mitochondrial genes to male versus female fitness variance. When mutant fitness effects are weakly correlated between the sexes, and the effective population size is large, mitochondrial genes should contribute much more to male than to female fitness variance. In contrast, high fitness correlations and small population sizes tend to equalize the contributions of mitochondrial genes to female versus male variance. We discuss implications of these results for the evolution of mitochondrial genome diversity and the genetic architecture of female and male fitness.     

Joint evolution of differential seed dispersal and self‐fertilization

Differential seed dispersal, in which selfed and outcrossed seeds possess different dispersal propensities, represents a potentially important individual‐level association. A variety of traits can mediate differential seed dispersal, including inflorescence and seed size variation. However, how natural selection shapes such associations is poorly known. Here, we developed theoretical models for the evolution of mating system and differential seed dispersal in metapopulations, incorporating heterogeneous pollination, dispersal cost, cost of outcrossing and environment‐dependent inbreeding depression. We considered three models. In the ‘fixed dispersal model’, only selfing rate is allowed to evolve. In the ‘fixed selfing model’, in which selfing is fixed but differential seed dispersal can evolve, we showed that natural selection favours a higher, equal or lower dispersal rate for selfed seeds to that for outcrossed seeds. However, in the ‘joint evolution model’, in which selfing and dispersal can evolve together, evolution necessarily leads to higher or equal dispersal rate for selfed seeds compared to that for outcrossed. Further comparison revealed that outcrossed seed dispersal is selected against by the evolution of mixed mating or selfing, whereas the evolution of selfed seed dispersal undergoes independent processes. We discuss the adaptive significance and constraints for mating system/dispersal association.     

metapop2: Re‐implementation of software for the analysis and management of subdivided populations using gene and allelic diversity

Management programmes often have to make decisions based on the analysis of the genetic properties and diversity of populations. Expected heterozygosity (or gene diversity) and population structure parameters are often used to make recommendations for conservation, such as avoidance of inbreeding or migration across subpopulations. Allelic diversity, however, can also provide complementary and useful information for conservation programmes, as it is highly sensitive to population bottlenecks, and is more related to long‐term selection response than heterozygosity. Here we present a completely revised and updated re‐implementation of the software metapop for the analysis of diversity in subdivided populations, as well as a tool for the management and dynamic estimation of optimal contributions in conservation programmes. This new update includes computation of allelic diversity for population analysis and management, as well as a simulation mode to forecast the consequences of taking different management strategies over time. Furthermore, the new implementation in C++ includes code optimization and improved memory usage, allowing for fast analysis of large data sets including single nucleotide polymorphism markers, as well as enhanced cross‐software and cross‐platform compatibility.     

The evolution of cooperation by the Hankshaw effect

The evolution of cooperation—costly behavior that benefits others—faces one clear obstacle. Namely, cooperators are always at a competitive disadvantage relative to defectors, individuals that reap the benefits, but evade the cost of cooperation. One solution to this problem involves genetic hitchhiking, where the allele encoding cooperation becomes linked to a beneficial mutation, allowing cooperation to rise in abundance. Here, we explore hitchhiking in the context of adaptation to a stressful environment by cooperators and defectors with spatially limited dispersal. Under such conditions, clustered cooperators reach higher local densities, thereby experiencing more mutational opportunities than defectors. Thus, the allele encoding cooperation has a greater probability of hitchhiking with alleles conferring stress adaptation. We label this probabilistic enhancement the “Hankshaw effect” after the character Sissy Hankshaw, whose anomalously large thumbs made her a singularly effective hitchhiker. Using an agent‐based model, we reveal a broad set of conditions that allow the evolution of cooperation through this effect. Additionally, we show that spite, a costly behavior that harms others, can evolve by the Hankshaw effect. While in an unchanging environment these costly social behaviors have transient success, in a dynamic environment, cooperation and spite can persist indefinitely.     

Self‐fertilization and inbreeding limit the scope for sexually antagonistic polymorphism

Sexual antagonism occurs when there is a positive intersexual genetic correlation in trait expression but opposite fitness effects of the trait(s) in males and females. As such, it constrains the evolution of sexual dimorphism and may therefore have implications for adaptive evolution. There is currently considerable evidence for the existence of sexually antagonistic genetic variation in laboratory and natural populations, but how sexual antagonism interacts with other evolutionary phenomena is still poorly understood in many cases. Here, we explore how self‐fertilization and inbreeding affect the maintenance of polymorphism for sexually antagonistic loci. We expected a priori that selfing should reduce the region of polymorphism, as inbreeding reduces the frequency of heterozygotes and speeds fixation. This expectation was supported, but although previous results suggest that the more an allele that is deleterious to one sex is dominant in that sex, the smaller the region of parameter space that will admit polymorphism, we found that this effect is weakened by self‐fertilization. However, the effect of inbreeding is not strong enough to completely cancel out the effect of dominance: For a given frequency of inbreeding, it will still be the case that the more dominant the alleles are in their deleterious context, the smaller the region of parameter space in which they can exist at polymorphism.     

HETEROZYGOSITY‐FITNESS CORRELATIONS: A TIME FOR REAPPRAISAL

Owing to the remarkable progress of molecular techniques, heterozygosity‐fitness correlations (HFCs) have become a popular tool to study the impact of inbreeding in natural populations. However, their underlying mechanisms are often hotly debated. Here we argue that these “debates” rely on verbal arguments with no basis in existing theory and inappropriate statistical testing, and that it is time to reconcile HFC with its historical and theoretical fundaments. We show that available data are quantitatively and qualitatively consistent with inbreeding‐based theory. HFC can be used to estimate the impact of inbreeding in populations, although such estimates are bound to be imprecise, especially when inbreeding is weak. Contrary to common belief, linkage disequilibrium is not an alternative to inbreeding, but rather comes with some forms of inbreeding, and is not restricted to closely linked loci. Finally, the contribution of local chromosomal effects to HFC, while predicted by inbreeding theory, is expected to be small, and has rarely if ever proven statistically significant using adequate tests. We provide guidelines to safely interpret and quantify HFCs, and present how HFCs can be used to quantify inbreeding load and unravel the structure of natural populations.     

Multiple losses of self‐incompatibility in North‐American Arabidopsis lyrata?: Phylogeographic context and population genetic consequences

Arabidopsis lyrata is mostly outcrossing due to a sporophytic self‐incompatibility (SI) system but around the Great Lakes of North America some populations have experienced a loss of SI. We researched the loss of SI in a phylogeographic context. We used cpDNA and microsatellite markers to test if populations of North‐American A. lyrata around the Great Lakes have experienced different (recent) histories, and linked this with individually established selfing phenotype and population level realized outcrossing rates calculated based on variation in progeny arrays at multi‐locus microsatellite markers. We found three chloroplast haplotypes, in two of which the loss of self‐incompatibility had occurred independently. Shifts to high rates of inbreeding were most apparent in one of these lineages but individuals showing loss of SI occurred in all three. Self‐compatible individuals usually showed a reduction of observed heterozygosity (H_O) compared to outcrossing individuals. In the lineage that included the populations with the highest levels of inbreeding, this reduction was more substantial. This may indicate that the loss of SI in this lineage did not occur as recently as in the other lineage. The geographic distribution of the haplotypes suggested that there had been at least two independent colonization routes to the north of the Great Lakes following the last glaciation. This is consistent with postglacial migration patterns that have been suggested for other organisms with limited dispersal, such as reptiles and amphibians.     

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.     

IS LIFE IMPOSSIBLE? INFORMATION,SEX, AND THE ORIGIN OF COMPLEX ORGANISMS

The earliest organisms are thought to have had high mutation rates. It has been asserted that these high mutation rates would have severely limited the information content of early genomes. This has led to a well‐known “paradox” because, in contemporary organisms, the mechanisms that suppress mutations are quite complex and a substantial amount of information is required to construct these mechanisms. The paradox arises because it is not clear how efficient error‐suppressing mechanisms could have evolved, and thus allowed the evolution of complex organisms, at a time when mutation rates were too high to permit the maintenance of very substantial amounts of information within genomes. Here, we use concepts from the formal theory of information to calculate the amount of genomic information that can be maintained. We identify conditions under which much higher levels of genomic information can be maintained than previously considered possible among origin‐of‐life researchers. In particular, we find that the highest levels of information are maintained when many genotypes produce identical phenotypes, and when reproduction occasionally involves recombination between multiple parental genomes. There is a good reason to believe that these conditions are relevant for very early organisms, and thus the results presented may provide a solution to a long‐standing logical problem associated with the early evolution of life.     

Looking into the black box: simulating the role of self‐fertilization and mortality in the genetic structure of Macrocystis pyrifera

Patterns of spatial genetic structure (SGS), typically estimated by genotyping adults, integrate migration over multiple generations and measure the effective gene flow of populations. SGS results can be compared with direct ecological studies of dispersal or mating system to gain additional insights. When mismatches occur, simulations can be used to illuminate the causes of these mismatches. Here, we report a SGS and simulation‐based study of self‐fertilization in Macrocystis pyrifera, the giant kelp. We found that SGS is weaker than expected in M. pyrifera and used computer simulations to identify selfing and early mortality rates for which the individual heterozygosity distribution fits that of the observed data. Only one (of three) population showed both elevated kinship in the smallest distance class and a significant negative slope between kinship and geographical distance. All simulations had poor fit to the observed data unless mortality due to inbreeding depression was imposed. This mortality could only be imposed for selfing, as these were the only simulations to show an excess of homozygous individuals relative to the observed data. Thus, the expected data consistently achieved nonsignificant differences from the observed data only under models of selfing with mortality, with best fits between 32% and 42% selfing. Inbreeding depression ranged from 0.70 to 0.73. The results suggest that density‐dependent mortality of early life stages is a significant force in structuring Macrocystis populations, with few highly homozygous individuals surviving. The success of these results should help to validate simulation approaches even in data‐poor systems, as a means to estimate otherwise difficult‐to‐measure life cycle parameters.     

Antibody‐mediated crosslinking of gut bacteria hinders the spread of antibiotic resistance

The body is home to a diverse microbiota, mainly in the gut. Resistant bacteria are selected by antibiotic treatments, and once resistance becomes widespread in a population of hosts, antibiotics become useless. Here, we develop a multiscale model of the interaction between antibiotic use and resistance spread in a host population, focusing on an important aspect of within‐host immunity. Antibodies secreted in the gut enchain bacteria upon division, yielding clonal clusters of bacteria. We demonstrate that immunity‐driven bacteria clustering can hinder the spread of a novel resistant bacterial strain in a host population. We quantify this effect both in the case where resistance preexists and in the case where acquiring a new resistance mutation is necessary for the bacteria to spread. We further show that the reduction of spread by clustering can be countered when immune hosts are silent carriers, and are less likely to get treated, and/or have more contacts. We demonstrate the robustness of our findings to including stochastic within‐host bacterial growth, a fitness cost of resistance, and its compensation. Our results highlight the importance of interactions between immunity and the spread of antibiotic resistance, and argue in the favor of vaccine‐based strategies to combat antibiotic resistance.     

Optimizing the genetic composition of a translocation population: Incorporating constraints and conflicting objectives

Translocations of threatened species can reduce the risk of extinction from a catastrophic event. For plants, translocation consists of moving individuals, seeds, or cuttings from a native (source) population to a new site. Ideally a translocation population would be genetically diverse and consist of fit founding individuals. In practice, there are challenges to designing such a population, including constraints on the availability of material, and tradeoffs between different goals. Here, we present an approach for designing a translocation population that identifies sets of founders that are optimized according to multiple criteria (e.g., genetic diversity), while also conforming to constraints on the representation of different founders (e.g., propagation success). It uses flexible inputs, including SNP genotypes, matrices of similarity between individuals, and vectors of phenotype data. We apply the approach to a critically endangered plant, Hibbertia puberula subsp. glabrescens (Dilleniaceae), which was genotyped at thousands of SNP loci. The goals of minimizing genetic similarity among the founding individuals and maximizing genetic diversity were largely complementary: populations optimized for one of these criteria were near‐optimal for the other. We also performed analyses in which we minimized genetic similarity among founding individuals while imposing selection (against hypothetical deleterious alleles, and against undesirable phenotypes, respectively), and here characterized sharp tradeoffs. This was useful in allowing the benefits of selection to be weighed against costs in terms of genetic similarity. In summary, we present an approach for designing a translocation population that allows flexible inputs, the imposition of realistic constraints, and examination of conflicting goals.     

Dobzhansky–Muller incompatibilities,dominance drive,and sex‐chromosome introgression at secondary contact zones: A simulation study

Dobzhansky–Muller (DM) incompatibilities involving sex chromosomes have been proposed to account for Haldane's rule (lowered fitness among hybrid offspring of the heterogametic sex) as well as Darwin's corollary (asymmetric fitness costs with respect to the direction of the cross). We performed simulation studies of a hybrid zone to investigate the effects of different types of DM incompatibilities on cline widths and positions of sex‐linked markers. From our simulations, X‐Y incompatibilities generate steep clines for both X‐linked and Y‐linked markers; random effects may produce strong noise in cline center positions when migration is high relative to fitness costs, but X‐ and Y‐centers always coincide strictly. X‐autosome and Y‐autosome incompatibilities also generate steep clines, but systematic shifts in cline centers occur when migration is high relative to selection, as a result of a dominance drive linked to Darwin's corollary. Interestingly, sex‐linked genes always show farther introgression than the associated autosomal genes. We discuss ways of disentangling the potentially confounding effects of sex biases in migration, we compare our results to those of a few documented contact zones, and we stress the need to study independent replicates of the same contact zone.     

The divergence history of the perennial plant Linaria cavanillesii confirms a recent loss of self‐incompatibility

Many angiosperms prevent inbreeding through a self‐incompatibility (SI) system, but the loss of SI has been frequent in their evolutionary history. The loss of SI may often lead to an increase in the selfing rate, with the purging of inbreeding depression and the ultimate evolution of a selfing syndrome, where plants have smaller flowers with reduced pollen and nectar production. In this study, we used approximate Bayesian computation (ABC) to estimate the timing of divergence between populations of the plant Linaria cavanillesii that differ in SI status and in which SI is associated with low inbreeding depression but not with a transition to full selfing or a selfing syndrome. Our analysis suggests that the mixed‐mating self‐compatible (SC) population may have begun to diverge from the SI populations around 2810 generation ago, a period perhaps too short for the evolution of a selfing syndrome. We conjecture that the SC population of L. cavanillesii is at an intermediate stage of transition between outcrossing and selfing.     

FISHER'S GEOMETRIC MODEL WITH A MOVING OPTIMUM

Fisher's geometric model has been widely used to study the effects of pleiotropy and organismic complexity on phenotypic adaptation. Here, we study a version of Fisher's model in which a population adapts to a gradually moving optimum. Key parameters are the rate of environmental change, the dimensionality of phenotype space, and the patterns of mutational and selectional correlations. We focus on the distribution of adaptive substitutions, that is, the multivariate distribution of the phenotypic effects of fixed beneficial mutations. Our main results are based on an “adaptive‐walk approximation,” which is checked against individual‐based simulations. We find that (1) the distribution of adaptive substitutions is strongly affected by the ecological dynamics and largely depends on a single composite parameter γ, which scales the rate of environmental change by the “adaptive potential” of the population; (2) the distribution of adaptive substitution reflects the shape of the fitness landscape if the environment changes slowly, whereas it mirrors the distribution of new mutations if the environment changes fast; (3) in contrast to classical models of adaptation assuming a constant optimum, with a moving optimum, more complex organisms evolve via larger adaptive steps.     

Family level inbreeding depression and the evolution of plant mating systems

Variation in the magnitude of inbreeding depression (ID) among families may have important consequences for mating system evolution. Experimental studies have shown that such variation is a common feature of natural plant populations. Unfortunately, the genetic and evolutionary significance of family level estimates remains obscure. Almost any kind of genetic variation will generate differences in ID among families, and as a consequence, a non-zero variance in family level ID is not sufficient to distinguish genetic architectures with wholly different implications for mating system evolution. Quantitative genetic methods provide a means to extract more information from ID experiments. Estimates of quantitative genetic variance components directly inform questions about the genetic basis of ID and should ultimately allow tests of alternative theories of mating system evolution.     

Genetic and demographic founder effects have long‐term fitness consequences for colonising populations

Colonisation is a fundamental ecological and evolutionary process that drives the distribution and abundance of organisms. The initial ability of colonists to establish is determined largely by the number of founders and their genetic background. We explore the importance of these demographic and genetic properties for longer term persistence and adaptation of populations colonising a novel habitat using experimental populations of Tribolium castaneum. We introduced individuals from three genetic backgrounds (inbred – outbred) into a novel environment at three founding sizes (2–32), and tracked populations for seven generations. Inbreeding had negative effects, whereas outbreeding generally had positive effects on establishment, population growth and long‐term persistence. Severe bottlenecks due to small founding sizes reduced genetic variation and fitness but did not prevent adaptation if the founders originated from genetically diverse populations. Thus, we find important and largely independent roles for both demographic and genetic processes in driving colonisation success.     

The impact of bottlenecks on microbial survival,adaptation, and phenotypic switching in host–pathogen interactions

Microbial pathogens and viruses can often maintain sufficient population diversity to evade a wide range of host immune responses. However, when populations experience bottlenecks, as occurs frequently during initiation of new infections, pathogens require specialized mechanisms to regenerate diversity. We address the evolution of such mechanisms, known as stochastic phenotype switches, which are prevalent in pathogenic bacteria. We analyze a model of pathogen diversification in a changing host environment that accounts for selective bottlenecks, wherein different phenotypes have distinct transmission probabilities between hosts. We show that under stringent bottlenecks, such that only one phenotype can initiate new infections, there exists a threshold stochastic switching rate below which all pathogen lineages go extinct, and above which survival is a near certainty. We determine how quickly stochastic switching rates can evolve by computing a fitness landscape for the evolutionary dynamics of switching rates, and analyzing its dependence on both the stringency of bottlenecks and the duration of within‐host growth periods. We show that increasing the stringency of bottlenecks or decreasing the period of growth results in faster adaptation of switching rates. Our model provides strong theoretical evidence that bottlenecks play a critical role in accelerating the evolutionary dynamics of pathogens.