Epistasis for fitness means that the selective effect of a mutation is conditional on the genetic background in which it appears. Although epistasis is widely observed in nature, our understanding of its consequences for evolution by natural selection remains incomplete. In particular, much attention focuses only on its influence on the instantaneous rate of changes in frequency of selected alleles via epistatic contribution to the additive genetic variance for fitness. Thus, in this framework epistasis only has evolutionary importance if the interacting loci are simultaneously segregating in the population. However, the selective accessibility of mutational trajectories to high fitness genotypes may depend on the genetic background in which novel mutations appear, and this effect is independent of population polymorphism at other loci. Here we explore this second influence of epistasis on evolution by natural selection. We show that it is the consequence of a particular form of epistasis, which we designate sign epistasis. Sign epistasis means that the sign of the fitness effect of a mutation is under epistatic control; thus, such a mutation is beneficial on some genetic backgrounds and deleterious on others. Recent experimental innovations in microbial systems now permit assessment of the fitness effects of individual mutations on multiple genetic backgrounds. We review this literature and identify many examples of sign epistasis, and we suggest that the implications of these results may generalize to other organisms. These theoretical and empirical considerations imply that strong genetic constraint on the selective accessibility of trajectories to high fitness genotypes may exist and suggest specific areas of investigation for future research.

Fitness interactions between loci in the genome, or epistasis, can result in mutations that are individually deleterious but jointly beneficial. Such epistasis gives rise to multiple peaks on the genotypic fitness landscape. The problem of evolutionary escape from such local peaks has been a central problem of evolutionary genetics for at least 75 years. Much attention has focused on models of small populations, in which the sequential fixation of valley genotypes carrying individually deleterious mutations operates most quickly owing to genetic drift. However, valley genotypes can also be subject to mutation while transiently segregating, giving rise to copies of the high fitness escape genotype carrying the jointly beneficial mutations. In the absence of genetic recombination, these mutations may then fix simultaneously. The time for this process declines sharply with increasing population size, and it eventually comes to dominate evolutionary behavior. Here we develop an analytic expression for N_crit, the critical population size that defines the boundary between these regimes, which shows that both are likely to operate in nature. Frequent recombination may disrupt high-fitness escape genotypes produced in populations larger than N_crit before they reach fixation, defining a third regime whose rate again slows with increasing population size. We develop a novel expression for this critical recombination rate, which shows that in large populations the simultaneous fixation of mutations that are beneficial only jointly is unlikely to be disrupted by genetic recombination if their map distance is on the order of the size of single genes. Thus, counterintuitively, mass selection alone offers a biologically realistic resolution to the problem of evolutionary escape from local fitness peaks in natural populations.

Evolutionarily stable strategy (ESS) models are widely viewed as predicting the strategy of an individual that when monomorphic or nearly so prevents a mutant with any other strategy from entering the population. In fact, the prediction of some of these models is ambiguous when the predicted strategy is “mixed”, as in the case of a sex ratio, which may be regarded as a mixture of the subtraits “produce a daughter” and “produce a son.” Some models predict only that such a mixture be manifested by the population as a whole, that is, as an “evolutionarily stable state”; consequently, strategy monomorphism or polymorphism is consistent with the prediction. The hawk-dove game and the sex-ratio game in a panmictic population are models that make such a “degenerate” prediction. We show here that the incorporation of population finiteness into degenerate models has effects for and against the evolution of a monomorphism (an ESS) that are of equal order in the population size, so that no one effect can be said to predominate. Therefore, we used Monte Carlo simulations to determine the probability that a finite population evolves to an ESS as opposed to a polymorphism. We show that the probability that an ESS will evolve is generally much less than has been reported and that this probability depends on the population size, the type of competition among individuals, and the number of and distribution of strategies in the initial population. We also demonstrate how the strength of natural selection on strategies can increase as population size decreases. This inverse dependency underscores the incorrectness of Fisher's and Wright's assumption that there is just one qualitative relationship between population size and the intensity of natural selection.

We examined causes of speciation in asexual populations in both sympatry and parapatry, providing an alternative explanation for the speciation patterns reported by Dieckmann and Doebeli (1999) and Doebeli and Dieckmann (2003). Both in sympatry and parapatry, they find that speciation occurs relatively easily. We reveal that in the sympatric clonal model, the equilibrium distribution is continuous and the disruptive selection driving evolution of discrete clusters is only transient. Hence, if discrete phenotypes are to remain stable in the sympatric sexual model, there should be some source of nontransient disruptive selection that will drive evolution of assortment. We analyze sexually reproducing populations using the Bulmer's infinitesimal model and show that cost-free assortment alone leads to speciation and disruptive selection only arises when the optimal distribution cannot be matched—in this example, because the phenotypic range is limited. In addition, Doebeli and Dieckmann's analyses assumed a high genetic variance and a high mutation rate. Thus, these theoretical models do not support the conclusion that sympatric speciation is a likely outcome of competition for resources. In their parapatric model (Doebeli and Dieckmann 2003), clustering into distinct phenotypes is driven by edge effects, rather than by frequency-dependent competition.

Studies of sex allocation offer excellent opportunities for examining the constraints and limits on adaptation. A major topic of debate within this field concerns the extent to which the ability of individuals to adaptively manipulate their offspring sex ratio is determined by constraints such as the method of sex determination. We address this problem by comparing the extent of sex-ratio adjustment across taxa with different methods of sex determination, under the common selective scenario of interactions between relatives. These interactions comprise the following: local resource competition (LRC), local mate competition (LMC), and local resource enhancement (LRE). We found that: (1) species with supposedly constraining methods of sex determination showed consistent sex-ratio adjustment in the predicted direction; (2) vertebrates with chromosomal sex determination (CSD) showed less adjustment then haplodiploid invertebrates; (3) invertebrates with possibly constraining sex-determination mechanisms (CSD and pseudo-arrhenotoky) did not show less adjustment then haplodiploid invertebrates; (4) greater sex-ratio adjustment was seen in response to LRC and LMC than LRE; (5) greater sex-ratio adjustment was seen in response to interactions between relatives (LRC, LMC, and LRE) compared to responses to other environmental factors. Our results also illustrate the problem that sex-determination mechanism and selective pressure are confounded across taxa because vertebrates with CSD are influenced primarily by LRE whereas invertebrates are influenced by LRC and LMC. Overall, our analyses suggest that sex-allocation theory needs to consider simultaneously the influence of variable selection pressures and variable constraints when applying general theory to specific cases.

Hybrid sterility can have evolutionary significance and varies substantially by taxon, but few models attempt to predict or explain this variability. Hybrid sterility is commonly observed and develops early in isolation, at odds with straightforward models that predict it would develop slowly and rarely be seen. Meiotic drive might explain the rapid development of hybrid sterility, but drive is rarely observed, modifiers are expected to repress it, and no precise testable predictions are available. Here I develop population genetic models for the establishment of meiotic drive based on how it spreads by benefiting carrier gametes competing with noncarrier gametes from the same parent, or intraparental gamete competition. The resulting models predict that meiotic drive can often produce substantial hybrid sterility over time even in the presence of repressors, yet observable drive will be rare. They also make quantitative predictions of the degree of sterility based on observable parameters of reproductive ecology, including frequency of multiple mating, effective dispersal of offspring, and population size. Finally, they suggest explanations for the association of heterochromatin changes with speciation. Experimental evidence is discussed showing that drive alleles at least sometimes contribute to hybrid sterility.

Quantitative traits show abundant genetic, environmental, and phenotypic variance, yet if they are subject to stabilizing selection for an optimal phenotype, both the genetic and environmental components are expected to decline. The mechanisms that determine the level and maintenance of phenotypic variance are not yet fully understood. While there has been extensive study of mechanisms maintaining genetic variability, it has generally been assumed that environmental variance is not dependent on the genotype and therefore not subject to change. However, accumulating data suggest that the environmental variance is under some degree of genetic control. In this study, it is assumed accordingly that both the genotypic value (i.e., mean phenotypic value) and the variance of phenotypic value given genotypic value depend on the genotype. Two models are investigated as potentially able to explain the protected maintenance of environmental variance of quantitative traits under stabilizing selection. One is varying environment among generations such that both the optimal phenotype and the strength of the stabilizing selection vary between generations. The other is the cost of homogeneity, which is based on an assumption of an engineering cost of minimizing variability in development. It is shown that a small homogeneity cost is enough to maintain the observed levels of environmental variance, whereas a large amount of temporal variation in the optimal phenotype and the strength of selection would be necessary.

The age of the angiosperms has long been of interest to botanists and evolutionary biologists. Many early efforts to date the age of the angiosperms and evolutionary divergences within the angiosperm clade using a molecular clock have yielded age estimates that are grossly inconsistent with the fossil record. We investigated the age of angiosperms using Bayesian relaxed clock (BRC) and penalized likelihood (PL) approaches. Both of these methods allow the incorporation of multiple fossil constraints into the optimization procedure. The BRC method allows a range of values for among-lineage rate of substitution, from a nearly clocklike behavior to a condition in which each branch is allowed an optimal substitution rate, and also accounts for variation in molecular evolution across multiple genes. A topology derived from an analysis of genes from all three plant genomes for 71 taxa was used as a backbone. The effects on age estimates of different genes, single-gene versus concatenated datasets, and the inclusion and assumptions of fossils as age constraints were examined. In addition, the influence of prior distributions on estimates of divergence times was also explored. These results indicate that widely divergent age estimates can result from the different methods (198–139 million years ago), different sources of data (275–122 million years ago), and the inclusion of temporal constraints to topologies. Most dates, however, are between 180–140 million years ago, suggesting a Middle Jurassic-Early Cretaceous origin of flowering plants, predating the oldest unequivocal fossil angiosperms by about 45–5 million years. Nonetheless, these dates are consistent with other recent studies that have used methods that relax the assumption of a strict molecular clock and also agree with the hypothesis that the angiosperms may be somewhat older than the fossil record indicates.

Propagation through vegetative cuttings is a widely used technique that may bias estimates of genetic and environmental effects on plant growth. Leafy stem cuttings from 210 genotypes from eight populations of Salix pulchra were rooted and raised at three levels of nitrogen availability. Cuttings showed a complex suite of responses to vegetative propagation. Population and/or genotypic variation in response to vegetative propagation was observed in (1) retention of leaves during rooting, (2) date that cuttings resumed shoot growth after rooting, and (3) the frequency of cuttings that remained shoot dormant throughout the experiment. Nitrogen treatments also caused different responses to vegetative propagation, influencing date that cuttings resumed shoot growth and frequency of shoot dormancy. Because each of these responses had a direct effect on final plant size, I concluded that final size was a product of both differences among genotypes and treatments in plant growth rate, as well as genotype- and treatment-specific responses to vegetative propagation. This study shows that plant growth experiments can be designed to quantify responses to vegetative propagation and statistically remove these artifacts of propagation from estimates of genetic and environmental effects on plant growth.

Multilocus studies assessing patterns of nucleotide polymorphism within and among closely related species provide access to genealogical information bearing on demographic and geographic aspects of their speciation history. However, the technical difficulties in obtaining sufficient sequence data have severely limited this approach thus far, especially in outbred plant taxa. We employ the analytical framework of divergence population genetics in testing the isolation model of speciation in three self-incompatible species of wild tomatoes (clade Lycopersicon), in particular the assumption of divergence without gene flow. Based on DNA sequence data for 13 nuclear loci, average levels of silent polymorphism vary more than three-fold among species. We estimate a large effective population size for the ancestral species, quite similar to that of the highly polymorphic L. peruvianum. The other two species, however, exhibit concordant signatures of population-size reduction. These demographic inferences are biologically plausible and consistent with results obtained from standard neutrality tests. While the isolation model cannot be rejected by goodness-of-fit criteria, patterns of intragenic linkage disequilibrium in L. peruvianum are indicative of historical introgression at least in some regions of the genome. Considered jointly with the geographic pattern of postzygotic reproductive isolation, our results suggest that speciation occurred under residual gene flow, implying natural selection as one of the evolutionary forces driving the diversification of tomato lineages.

There is mounting evidence consistent with a general role of positive selection acting on the Drosophila melanogaster X-chromosome. However, this positive selection need not necessarily arise from forces that are adaptive to the organism. Nonadaptive meiotic drive may exist on the X-chromosome and contribute to forces of selection. Females from a reference D. melanogaster line, containing the X-linked marker white, were crossed to males from 49 isofemale lines established from seven African and five non-African natural populations to detect naturally occurring meiotic drive. Several lines exhibited a departure from expected Mendelian transmission of X-chromosomes to the third generation (F₂) offspring, particularly those from hybrid African male parents. F₂ viability was not correlated with skewed chromosomal inheritance. However, a significant difference in viability between cosmopolitan and tropical African crosses was observed. Recombination analysis supports the presence of a male-acting meiotic drive element near the centromeric region of the X-chromosome and putative recessive autosomal drive suppression. There is also evidence of another female-acting drive element linked to white. The possible role meiotic drive may contribute in shaping levels of genetic variation in D. melanogaster, and additional ways to test this hypothesis are discussed.

Patterns of investment of limiting resources in such processes as competing for food and defense against natural enemies are shaped by trade-offs and constraints. In Drosophila melanogaster artificial selection for increased resistance to parasitoids results in a correlated decrease in larval competitive ability. Here we ask whether selection for competitive ability leads to a correlated reduction in parasitoid resistance. Replicated lines of D. melanogaster were maintained under crowded or uncrowded conditions for eight generations. As expected, the crowded lines evolved higher competitive ability (when tested against a common strain of fly). But instead of parasitoid resistance decreasing, we found a significant increase, and that this was associated with elevated densities of haemocytes in second-instar larvae. To understand these results we measured a variety of life-history traits in the two sets of lines. We find evidence that directly and indirectly selected changes in competitive ability are due to different mechanisms. We also ask why crowded conditions should select for increased resistance to parasitism, and conclude that it is unlikely to be due to correlated selection for resistance to other natural enemies, but might be due to correlated selection for better wound responses.

“Peak shift” is a behavioral response bias arising from discrimination learning in which animals display a directional, but limited, preference for or avoidance of unusual stimuli. Its hypothesized evolutionary relevance has been primarily in the realm of aposematic coloration and limited sexual dimorphism. Here, we develop a novel functional approach to peak shift, based on signal detection theory, which characterizes the response bias as arising from uncertainty about stimulus appearance, frequency, and quality. This approach allows the influence of peak shift to be generalized to the evolution of signals in a variety of domains and sensory modalities. The approach is illustrated with a bumblebee (Bombus impatiens) discrimination learning experiment. Bees exhibited peak shift while foraging in an artificial Batesian mimicry system. Changes in flower abundance, color distribution, and visitation reward induced bees to preferentially visit novel flower colors that reduced the risk of flower-type misidentification. Under conditions of signal uncertainty, peak shift results in visitation to rarer, but more easily distinguished, morphological variants of rewarding species in preference to their average morphology. Peak shift is a common and taxonomically wide-spread phenomenon. This example of the possible role of peak shift in signal evolution can be generalized to other systems in which a signal receiver learns to make choices in situations in which signal variation is linked to the sender's reproductive success.

Mutual policing is an important mechanism for maintaining social harmony in group-living organisms. In some ants, bees, and wasps, workers police male eggs laid by other workers in order to maintain the reproductive primacy of the queen. Kin selection theory predicts that multiple mating by the queen is one factor that can selectively favor worker policing. This is because when the queen is mated to multiple males, workers are more closely related to queen's sons than to the sons of other workers. Here we provide an additional test of worker policing theory in Vespinae wasps. We show that the yellowjacket Vespula rufa is characterized by low mating frequency, and that a significant percentage of the males are workers' sons. This supports theoretical predictions for paternities below 2, and contrasts with other Vespula species, in which paternities are higher and few or no adult males are worker produced, probably due to worker policing, which has been shown in one species, Vespula vulgaris. Behavioral observations support the hypothesis that V. rufa has much reduced worker policing compared to other Vespula. In addition, a significant proportion of worker-laid eggs were policed by the queen.

Ehrlich and Raven's (1964) hypothesis on coevolution has stimulated numerous phylogenetic studies that focus on the effects of plant defensive chemistry as the main ecological axis of phytophagous insect diversification. However, other ecological features affect host use and diet breadth and they may have very different consequences for insect evolution. In this paper, we present a phylogenetic study based on DNA sequences from mitochondrial and protein-coding genes of species in the seed beetle genus Stator, which collectively show considerable interspecific variation in host affiliation, diet breadth, and the dispersal stage of the seeds that they attack. We used comparative analyses to examine transitions in these three axes of resource use. We argue that these analyses show that diet breadth evolution is dependent upon colonizing novel hosts that are closely or distantly related to the ancestral host, and that oviposition substrate affects the evolution of host-plant affiliation, the evolution of dietary specialization, and the degree to which host plants are shared between species. The results of this study show that diversification is structured by interactions between different selective pressures and along multiple ecological axes.

The analysis of interactions between lineages at varying levels of genetic divergence can provide insights into the process of speciation through the accumulation of incompatible mutations. Ring species, and especially the Ensatina eschscholtzii system exemplify this approach. The plethodontid salamanders E. eschscholtzii xanthoptica and E. eschscholtzii platensis hybridize in the central Sierran foothills of California. We compared the genetic structure across two transects (southern and northern Calaveras Co.), one of which was resampled over 20 years, and examined diagnostic molecular markers (eight allozyme loci and mitochondrial DNA) and a diagnostic quantitative trait (color pattern). Key results across all studies were: (1) cline centers for all markers were coincident and the zones were narrow, with width estimates of 730 m to 2000 m; (2) cline centers at the northern Calaveras transect were coincident between 1981 and 2001, demonstrating repeatability over five generations; (3) there were very few if any putative F₁s, but a relatively high number of backcrossed individuals in the central portion of transects; and (4) we found substantial linkage disequilibrium in all three studies and strong heterozygote deficit both in northern Calaveras, in 2001, and southern Calaveras. Both linkage disequilibrium and heterozygote deficit showed maximum values near the center of the zones. Using estimates of cline width and dispersal, we infer strong selection against hybrids. This is sufficient to promote accumulation of differences at loci that are neutral or under divergent selection, but would still allow for introgression of adaptive alleles. The evidence for strong but incomplete isolation across this centrally located contact is consistent with theory suggesting a gradual increase in postzygotic incompatibility between allopatric populations subject to divergent selection and reinforces the value of Ensatina as a system for the study of divergence and speciation at multiple stages.

All-hybrid populations of the water frog, Rana esculenta, are exceptional in consisting of independently and to some extent sexually reproducing interspecific hybrids. In most of its range R. esculenta reproduces hemiclonally with one of the parental species, R. lessonae or R. ridibunda, but viable populations of diploid and triploid hybrids, in which no individuals of the parental species have been found, exist in the northern part of the range. We test the hypothesis that nonhybrids arise every year in these all-hybrid populations, but die during larval development. Microsatellite markers were used to determine the genotypes of adults and abnormal and healthy offspring in three all-hybrid populations of R. esculenta in Denmark. Of all eggs and larvae, 63% developed abnormally or died, with some being nonhybrid (genomes matching one of the parental species), many being aneuploid (with noninteger chromosome sets), a few being tetraploid, and many eggs possibly being unfertilized. The 37% surviving and apparently healthy froglets were all diploid or triploid hybrids. In all three populations, gametogenesis matched the pattern previously described for all-hybrid R. esculenta populations in which most triploid adults have two R. lessonae genomes. This pattern was surprising for the one population in which triploid adults had two R. ridibunda genomes, because here it leads to a deficiency of gametes with an R. lessonae genome and should compromise the stability of this population. We conclude that faulty gametogenesis and mating between frogs with incompatible gametes induce a significant hybrid load in all-hybrid populations of R. esculenta, and we discuss compensating advantages and potential evolutionary trajectories to reduce this hybrid load.

Many morphological and life-history traits show phenotypic plasticity that can be described by reaction norms, but few studies have attempted individual-level analyses of reaction norms in the wild. We analyzed variation in individual reaction norms between laying date and three climatic variables (local temperature, local rainfall, and North Atlantic Oscillation) of 1126 female collared flycatchers (Ficedula albicollis) with a restricted maximum likehood linear mixed model approach using random-effect best linear unbiased predictor estimates for the elevation (i.e., expected laying date in the average environment) and slope (i.e., adjustment in laying date as a function of environment) of females' reaction norms. Variation in laying date was best explained by local temperature, and individual females differed in both the elevation and the slope of their laying date–temperature reaction norms. As revealed by animal model analyses, there was weak evidence for additive genetic variance of elevation (h² ± SE = 0.09 ± 0.09), whereas there was no evidence for heritability of slope (h² ± SE = 0.00 ± 0.01). Selection analysis, using a female's lifetime production of fledglings or recruits as an estimate of her fitness, revealed significant selection for a lower phenotypic value and breeding value for elevation (i.e., earlier laying date at the average temperature). There was selection for steeper phenotypic values of slope (i.e., greater plasticity in the adjustment of laying date to temperature), but no significant selection on the breeding values of slope. Although these results suggest that phenotypic laying date is influenced by additive genetic factors, as well as by an interaction with the environment, selection on plasticity would not produce an evolutionary response.

Genetic theory predicts that directional selection should deplete additive genetic variance for traits closely related to fitness, and may favor the maintenance of alleles with antagonistically pleiotropic effects on fitness-related traits. Trait heritability is therefore expected to decline with the degree of association with fitness, and some genetic correlations between selected traits are expected to be negative. Here we demonstrate a negative relationship between trait heritability and association with lifetime reproductive success in a wild population of bighorn sheep (Ovis canadensis) at Ram Mountain, Alberta, Canada. Lower heritability for fitness-related traits, however, was not wholly a consequence of declining genetic variance, because those traits showed high levels of residual variance. Genetic correlations estimated between pairs of traits with significant heritability were positive. Principal component analyses suggest that positive relationships between morphometric traits constitute the main axis of genetic variation. Trade-offs in the form of negative genetic or phenotypic correlations among the traits we have measured do not appear to constrain the potential for evolution in this population.