Demography, pollination, and Baker's Law

Baker's Law states that selfing should commonly be selected during dispersal because bottlenecks during colonization limit the availability of mates. Although this truism has broad intuitive appeal, a recent body of theory (Cheptou and Massol 2009; Massol and Cheptou 2011) casts doubt on whether adaptation favors both selfing and dispersal when both parameters are free to evolve. In these models, the joint evolution of dispersal and the selfing rate are considered in a metapopulation, with a spatially and temporally variable pollination environment. Under these conditions, adaptation favors one of two strategies: the "dispersal/outcrosser" syndrome and the "no dispersal/selfing" syndrome. These results appear to contradict the prediction of Baker's Law. These models clarify how variation in the pollination environment per se cannot generate an association between selfing and dispersal. That being said, demographic factors during dispersal episodes are likely to be important in generating patterns consistent with Baker's law. Determining whether Baker's law maintains its predictive utility requires determining whether seed banks, the perennial habit, multiple introductions, or the simultaneous arrival of many founders weaken selection for selfing during the bottleneck associated with a dispersal event. These issues highlight the many assumptions that are necessary for Baker's law to hold.     

Adaptation of Drosophila to a novel laboratory environment reveals temporally heterogeneous trajectories of selected alleles

The genomic basis of adaptation to novel environments is a fundamental problem in evolutionary biology that has gained additional importance in the light of the recent global change discussion. Here, we combined laboratory natural selection (experimental evolution) in Drosophila melanogaster with genome‐wide next generation sequencing of DNA pools (Pool‐Seq) to identify alleles that are favourable in a novel laboratory environment and traced their trajectories during the adaptive process. Already after 15 generations, we identified a pronounced genomic response to selection, with almost 5000 single nucleotide polymorphisms (SNP; genome‐wide false discovery rates < 0.005%) deviating from neutral expectation. Importantly, the evolutionary trajectories of the selected alleles were heterogeneous, with the alleles falling into two distinct classes: (i) alleles that continuously rise in frequency; and (ii) alleles that at first increase rapidly but whose frequencies then reach a plateau. Our data thus suggest that the genomic response to selection can involve a large number of selected SNPs that show unexpectedly complex evolutionary trajectories, possibly due to nonadditive effects.     

Diversification across a heterogeneous landscape

Adaptation to contrasting environments across a heterogeneous landscape favors the formation of ecotypes by promoting ecological divergence. Patterns of fitness variation in the field can show whether natural selection drives local adaptation and ecotype formation. However, to demonstrate a link between ecological divergence and speciation, local adaptation must have consequences for reproductive isolation. Using contrasting ecotypes of an Australian wildflower, Senecio lautus in common garden experiments, hybridization experiments, and reciprocal transplants, we assessed how the environment shapes patterns of adaptation and the consequences of adaptive divergence for reproductive isolation. Local adaptation was strong between ecotypes, but weaker between populations of the same ecotype. F1 hybrids exhibited heterosis, but crosses involving one native parent performed better than those with two foreign parents. In a common garden experiment, F2 hybrids exhibited reduced fitness compared to parentals and F1 hybrids, suggesting that few genetic incompatibilities have accumulated between populations adapted to contrasting environments. Our results show how ecological differences across the landscape have created complex patterns of local adaptation and reproductive isolation, suggesting that divergent natural selection has played a fundamental role in the early stages of species diversification.     

Evolution of Cooperation in a Heterogeneous Graph: Fixation Probabilities under Weak Selection

It has been shown that natural selection favors cooperation in a homogenous graph if the benefit-to-cost ratio exceeds the degree of the graph. However, most graphs related to interactions in real populations are heterogeneous, in which some individuals have many more neighbors than others. In this paper, we introduce a new state variable to measure the time evolution of cooperation in a heterogeneous graph. Based on the diffusion approximation, we find that the fixation probability of a single cooperator depends crucially on the number of its neighbors. Under weak selection, a cooperator with more neighbors has a larger probability of fixation in the population. We then investigate the average fixation probability of a randomly chosen cooperator. If a cooperator pays a cost for each of its neighbors (the so called fixed cost per game case), natural selection favors cooperation if the benefit-to-cost ratio is larger than the average degree. In contrast, if a cooperator pays a fixed cost and all its neighbors share the benefit (the fixed cost per individual case), cooperation is favored if the benefit-to-cost ratio is larger than the harmonic mean of the degree distribution. Moreover, increasing the graph heterogeneity will reduce the effect of natural selection.     

Evolutionary inevitability of sexual antagonism

Sexual antagonism, whereby mutations are favourable in one sex and disfavourable in the other, is common in natural populations, yet the root causes of sexual antagonism are rarely considered in evolutionary theories of adaptation. Here, we explore the evolutionary consequences of sex-differential selection and genotype-by-sex interactions for adaptation in species with separate sexes. We show that sexual antagonism emerges naturally from sex differences in the direction of selection on phenotypes expressed by both sexes or from sex-by-genotype interactions affecting the expression of such phenotypes. Moreover, modest sex differences in selection or genotype-by-sex effects profoundly influence the long-term evolutionary trajectories of populations with separate sexes, as these conditions trigger the evolution of strong sexual antagonism as a by-product of adaptively driven evolutionary change. The theory demonstrates that sexual antagonism is an inescapable by-product of adaptation in species with separate sexes, whether or not selection favours evolutionary divergence between males and females.     

Correlated responses to clonal selection in populations of Daphnia pulicaria: mechanisms of genetic correlation and the creative power of sex

Genetic correlations among traits alter evolutionary trajectories due to indirect selection. Pleiotropy, chance linkage, and selection can all lead to genetic correlations, but have different consequences for phenotypic evolution. We sought to assess the mechanisms contributing to correlations with size at maturity in the cyclic parthenogen Daphnia pulicaria. We selected on size in each of four populations that differ in the frequency of sex, and evaluated correlated responses in a life table. Size at advanced adulthood, reproductive output, and adult growth rate clearly showed greater responses in high‐sex populations, with a similar pattern in neonate size and r. This pattern is expected only when trait correlations are favored by selection and the frequency of sex favors the creation and demographic expansion of highly fit clones. Juvenile growth and age at maturity did not diverge consistently. The inter‐clutch interval appeared to respond more strongly in low‐sex populations, but this was not statistically significant. Our data support the hypothesis that correlated selection is the strongest driver of genetic correlations, and suggest that in organisms with both sexual and asexual reproduction, adaptation can be enhanced by recombination.     

The Distribution of Fitness Effects of Beneficial Mutations in Pseudomonas aeruginosa

Understanding how beneficial mutations affect fitness is crucial to our understanding of adaptation by natural selection. Here, using adaptation to the antibiotic rifampicin in the opportunistic pathogen Pseudomonas aeruginosa as a model system, we investigate the underlying distribution of fitness effects of beneficial mutations on which natural selection acts. Consistent with theory, the effects of beneficial mutations are exponentially distributed where the fitness of the wild type is moderate to high. However, when the fitness of the wild type is low, the data no longer follow an exponential distribution, because many beneficial mutations have large effects on fitness. There is no existing population genetic theory to explain this bias towards mutations of large effects, but it can be readily explained by the underlying biochemistry of rifampicin–RNA polymerase interactions. These results demonstrate the limitations of current population genetic theory for predicting adaptation to severe sources of stress, such as antibiotics, and they highlight the utility of integrating statistical and biophysical approaches to adaptation.     

The intensity of sexual selection predicts weapon size in male bovids

As a classical example of a sexually selected trait, the horns of male bovids offer a prime opportunity to identify predictors of the intensity of sexual selection. Here I use the comparative method to quantify sexual and natural selection pressures behind interspecific variation in horn length. I show that male horn length depends on factors proposed to affect the mean mate number per mating male, correlating positively with group size and negatively with male territoriality. This suggests that whereas group size increases the opportunity for sexual selection, territoriality reduces it because territorial males are unable to follow and monopolize female groups as effectively as males in nonterritorial species. Sexual body size dimorphism also correlates positively with group size and negatively with territoriality, corroborating these factors as predictors of the intensity of sexual selection on males. Female horn length was unaffected by the factors related to mating system, suggesting that this trait is mainly under natural selection. Using female horn length as a proxy for forces of natural selection revealed a negative effect on male horn length. Thus where natural selection favors female horns, possibly as effective weapons against predators, a similar selection pressure on males might prevent them from evolving too elaborate horns through sexual selection. There was no correlation found between horn length and latitude, thus providing no support for the hypothesis that horns have a thermoregulatory function.     

Indirect selection of implicit mutation protocols

A hypothesis that mutability evolves to facilitate evolutionary adaptation is dismissed by many biologists. Their skepticism is based on a theoretical expectation that natural selection must minimize mutation rates. That view, in turn, is historically grounded in an intuitive presumption that "the vast majority of mutations are harmful." But such skepticism is surely misplaced. Several highly mutagenic genomic patterns, including simple sequence repeats, and transposable elements, are integrated into an unexpectedly large proportion of functional genetic loci. Because alleles arising within such patterns can retain an intrinsic propensity toward a particular style of mutation, natural selection that favors any such allele can indirectly favor the site's mutability as well. By exploiting patterns that have produced beneficial alleles in the past, indirect selection can encourage mutation within constraints that reduce the probability of deleterious effect, thereby shaping implicit "mutation protocols" that effectively promote evolvability.     

Fast Evolution from Precast Bricks: Genomics of Young Freshwater Populations of Threespine Stickleback Gasterosteus aculeatus

Adaptation is driven by natural selection; however, many adaptations are caused by weak selection acting over large timescales, complicating its study. Therefore, it is rarely possible to study selection comprehensively in natural environments. The threespine stickleback (Gasterosteus aculeatus) is a well-studied model organism with a short generation time, small genome size, and many genetic and genomic tools available. Within this originally marine species, populations have recurrently adapted to freshwater all over its range. This evolution involved extensive parallelism: pre-existing alleles that adapt sticklebacks to freshwater habitats, but are also present at low frequencies in marine populations, have been recruited repeatedly. While a number of genomic regions responsible for this adaptation have been identified, the details of selection remain poorly understood. Using whole-genome resequencing, we compare pooled genomic samples from marine and freshwater populations of the White Sea basin, and identify 19 short genomic regions that are highly divergent between them, including three known inversions. 17 of these regions overlap protein-coding genes, including a number of genes with predicted functions that are relevant for adaptation to the freshwater environment. We then analyze four additional independently derived young freshwater populations of known ages, two natural and two artificially established, and use the observed shifts of allelic frequencies to estimate the strength of positive selection. Adaptation turns out to be quite rapid, indicating strong selection acting simultaneously at multiple regions of the genome, with selection coefficients of up to 0.27. High divergence between marine and freshwater genotypes, lack of reduction in polymorphism in regions responsible for adaptation, and high frequencies of freshwater alleles observed even in young freshwater populations are all consistent with rapid assembly of G. aculeatus freshwater genotypes from pre-existing genomic regions of adaptive variation, with strong selection that favors this assembly acting simultaneously at multiple loci.     

CONVERGENCE AND DIVERGENCE DURING THE ADAPTATION TO SIMILAR ENVIRONMENTS BY AN AUSTRALIAN GROUNDSEL

Adaptation to replicate environments is often achieved through similar phenotypic solutions. Whether selection also produces convergent genomic changes in these situations remains largely unknown. The variable groundsel, Senecio lautus, is an excellent system to investigate the genetic underpinnings of convergent evolution, because morphologically similar forms of these plants have adapted to the same environments along the coast of Australia. We compared range‐wide patterns of genomic divergence in natural populations of this plant and searched for regions putatively affected by natural selection. Our results indicate that environmental adaptation followed complex genetic trajectories, affecting multiple loci, implying both the parallel recruitment of the same alleles and the divergence of completely different genomic regions across geography. An analysis of the biological functions of candidate genes suggests that adaptation to coastal environments may have occurred through the recruitment of different genes participating in similar processes. The relatively low genetic convergence that characterizes the parallel evolution of S. lautus forms suggests that evolution is more constrained at higher levels of biological organization.     

Genetic correlations and sex‐specific adaptation in changing environments

Females and males have conflicting evolutionary interests. Selection favors the evolution of different phenotypes within each sex, yet divergence between the sexes is constrained by the shared genetic basis of female and male traits. Current theory predicts that such “sexual antagonism” should be common: manifesting rapidly during the process of adaptation, and slow in its resolution. However, these predictions apply in temporally stable environments. Environmental change has been shown empirically to realign the direction of selection acting on shared traits and thereby alleviate signals of sexually antagonistic selection. Yet there remains no theory for how common sexual antagonism should be in changing environments. Here, we analyze models of sex‐specific evolutionary divergence under directional and cyclic environmental change, and consider the impact of genetic correlations on long‐run patterns of sex‐specific adaptation. We find that environmental change often aligns directional selection between the sexes, even when they have divergent phenotypic optima. Nevertheless, some forms of environmental change generate persistent sexually antagonistic selection that is difficult to resolve. Our results reinforce recent empirical observations that changing environmental conditions alleviate conflict between males and females. They also generate new predictions regarding the scope for sexually antagonistic selection and its resolution in changing environments.     

Evolutionary feedback mediated through population density, illustrated with viruses in chemostats

A cornerstone of evolutionary ecology is that population density affects adaptation: r and K selection is the obvious example. The reverse is also appreciated: adaptation impacts population density. Yet, empirically demonstrating a direct connection between population density and adaptation is challenging. Here, we address both evolution and ecology of population density in models of viral (bacteriophage) chemostats. Chemostats supply nutrients for host cell growth, and the hosts are prey for viral reproduction. Two different chemostat designs have profoundly different consequences for viral evolution. If host and virus are confined to the same chamber, as in a predator-prey system, viral regulation of hosts feeds back to maintain low viral density (measured as infections per cell). Viral adaptation impacts host density but has a small effect on equilibrium viral density. More interesting are chemostats that supply the viral population with hosts from a virus-free refuge. Here, a type of evolutionary succession operates: adaptation at low viral density leads to higher density, but high density then favors competitive ability. Experiments support these models with both phenotypic and molecular data. Parallels to these designs exist in many natural systems, so these experimental systems may yield insights to the evolution and regulation of natural populations.     

Experimental evolution of slowed cognitive aging in Drosophila melanogaster

Reproductive output and cognitive performance decline in parallel during aging, but it is unknown whether this reflects a shared genetic architecture or merely the declining force of natural selection acting independently on both traits. We used experimental evolution in Drosophila melanogaster to test for the presence of genetic variation for slowed cognitive aging, and assess its independence from that responsible for other traits’ decline with age. Replicate experimental populations experienced either joint selection on learning and reproduction at old age (Old + Learning), selection on late‐life reproduction alone (Old), or a standard two‐week culture regime (Young). Within 20 generations, the Old + Learning populations evolved a slower decline in learning with age than both the Old and Young populations, revealing genetic variation for cognitive aging. We found little evidence for a genetic correlation between cognitive and demographic aging: although the Old + Learning populations tended to show higher late‐life fecundity than Old populations, they did not live longer. Likewise, selection for late reproduction alone did not result in improved late‐life learning. Our results demonstrate that Drosophila harbor genetic variation for cognitive aging that is largely independent from genetic variation for demographic aging and suggest that these two aspects of aging may not necessarily follow the same trajectories.     

Host Adaptation Is Contingent upon the Infection Route Taken by Pathogens

Evolution of pathogen virulence is affected by the route of infection. Also, alternate infection routes trigger different physiological responses on hosts, impinging on host adaptation and on its interaction with pathogens. Yet, how route of infection may shape adaptation to pathogens has not received much attention at the experimental level. We addressed this question through the experimental evolution of an outbred Drosophila melanogaster population infected by two different routes (oral and systemic) with Pseudomonas entomophila. The two selection regimes led to markedly different evolutionary trajectories. Adaptation to infection through one route did not protect from infection through the alternate route, indicating distinct genetic bases. Finally, relatively to the control population, evolved flies were not more resistant to bacteria other than Pseudomonas and showed higher susceptibility to viral infections. These specificities and trade-offs may contribute to the maintenance of genetic variation for resistance in natural populations. Our data shows that the infection route affects host adaptation and thus, must be considered in studies of host-pathogen interaction.     

The roles of natural and sexual selection during adaptation to a novel environment

The net effect of sexual selection on nonsexual fitness is controversial. On one side, elaborate display traits and preferences for them can be costly, reducing the nonsexual fitness of individuals possessing them, as well as their offspring. In contrast, sexual selection may reinforce nonsexual fitness if an individual's attractiveness and quality are genetically correlated. According to recent models, such good-genes mate choice should increase both the extent and rate of adaptation. We evolved 12 replicate populations of Drosophila serrata in a powerful two-way factorial experimental design to test the separate and combined contributions of natural and sexual selection to adaptation to a novel larval food resource. Populations evolving in the presence of natural selection had significantly higher mean nonsexual fitness when measured over three generations (13-15) during the course of experimental evolution (16-23% increase). The effect of natural selection was even more substantial when measured in a standardized, monogamous mating environment at the end of the experiment (generation 16; 52% increase). In contrast, and despite strong sexual selection on display traits, there was no evidence from any of the four replicate fitness measures that sexual selection promoted adaptation. In addition, a comparison of fitness measures conducted under different mating environments demonstrated a significant direct cost of sexual selection to females, likely arising from some form of male-induced harm. Indirect benefits of sexual selection in promoting adaptation to this novel resource environment therefore appear to be absent in this species, despite prior evidence suggesting the operation of good-genes mate choice in their ancestral environment. How novel environments affect the operation of good-genes mate choice is a fundamental question for future sexual selection research.     

CORRELATIONAL SELECTION FOR COLOR PATTERN AND ANTIPREDATOR BEHAVIOR IN THE GARTER SNAKE THAMNOPHIS ORDINOIDES

Correlational selection favors combinations of traits and is a key element of many models of phenotypic and genetic evolution. Multiple regression techniques for measuring selection allow for the direct estimation of correlational selection gradients, yet few studies in natural populations have investigated this process. Color patterns and antipredator behaviors of snakes are thought to function interactively in predator escape and therefore may be subject to correlational selection. To investigate this hypothesis, I studied the survivorship of juvenile garter snakes, Thamnophis ordinoides, as a function of a suite of escape behaviors and color pattern. The only natural selection detected favored opposite combinations of stripedness of the color pattern and the tendency to perform during escape evasive behaviors called reversals. This selection presumably results from optical illusions created by moving patterns and their effects on visually foraging predators. Analysis of the bivariate selection surface shows that pure correlational selection can be thought of as a series of linear selection functions on one trait whose slopes depend on the value of the second trait. Alternatively, viewing the selection surface along its major axes reveals stabilizing and disruptive components of correlational selection. It is further shown that correlational selection alone can promote genetic variance and covariance within a generation. This phenomenon may be partially responsible for the extreme variation in color pattern and the genetic covariance between color pattern and behavior observed in natural populations of T. ordinoides.     

Repeated and predictable patterns of ecotypic differentiation during a biological invasion: lake–stream divergence in parapatric Swiss stickleback

The relative importance of ecological selection and geographical isolation in promoting and constraining genetic and phenotypic differentiation among populations is not always obvious. Interacting with divergent selection, restricted opportunity for gene flow may in some cases be as much a cause as a consequence of adaptation, with the latter being a hallmark of ecological speciation. Ecological speciation is well studied in parts of the native range of the three‐spined stickleback. Here, we study this process in a recently invaded part of its range. Switzerland was colonized within the past 140 years from at least three different colonization events involving different stickleback lineages. They now occupy diverse habitats, ranging from small streams to the pelagic zone of large lakes. We use replicated systems of parapatric lake and stream populations, some of which trace their origins to different invasive lineages, to ask (i) whether phenotypic divergence occurred among populations inhabiting distinct habitats, (ii) whether trajectories of phenotypic divergence follow predictable parallel patterns and (iii) whether gene flow constrains divergent adaptation or vice versa. We find consistent phenotypic divergence between populations occupying distinct habitats. This involves parallel evolution in several traits with known ecological relevance in independent evolutionary lineages. Adaptive divergence supersedes homogenizing gene flow even at a small spatial scale. We find evidence that adaptive phenotypic divergence places constraints on gene flow over and above that imposed by geographical distance, signalling the early onset of ecological speciation.     

Do evolutionary processes minimize expected losses?

Evolution by variation and natural selection is often viewed as an optimization process that favors those organisms which are best adapted to their environment. This leaves open the issue of how to measure adaptation and what criterion is implied for optimization. This problem has been framed and analysed mathematically under the assumption that individuals compete to minimize expected losses across a series of decisions (e.g. choice of behavior), where each decision offers a stochastic payoff. But the fact that a particular analysis is tractable for a specified criterion does not imply the fidelity of that criterion. Computer simulations involving a version of the k -armed bandit problem can address the veracity of the hypothesis that individuals are selected to minimize expected losses. The results offered here do not support this hypothesis.     

Levels of selection and the formal Darwinism project

Understanding good design requires addressing the question of what units undergo natural selection, thereby becoming adapted. There is, therefore, a natural connection between the formal Darwinism project (which aims to connect population genetics with the evolution of design and fitness maximization) and levels of selection issues. We argue that the formal Darwinism project offers contradictory and confusing lines of thinking concerning level(s) of selection. The project favors multicellular organisms over both the lower (cell) and higher (social group) levels as the level of adaptation. Grafen offers four reasons for giving such special status to multicellular organisms: (1) they lack appreciable within-organism cell selection, (2) they have multiple features that appear contrived for the same purpose, (3) they possess a set of phenotypes, and (4) they leave offspring according to their phenotypes. We discuss why these rationales are not compelling and suggest that a more even-handed approach, in which multicellular organisms are not assumed to have special status, would be desirable for a project that aims to make progress on the foundations of evolutionary theory.