Bateman's classic paper on fly mating systems inspired quantitative study of sexual selection but also resulted in much debate and confusion. Here, I consider the meaning of Bateman's principles in the context of selection theory. Success in precopulatory sexual selection can be quantified as a “mating differential,” which is the covariance between trait values and relative mating success. The mating differential is converted into a selection differential by the Bateman gradient, which is the least squares regression of relative reproductive success on relative mating success. Hence, a complete understanding of precopulatory sexual selection requires knowledge of two equally important aspects of mating patterns: the mating differential, which requires a focus on mechanisms generating covariance between trait values and mating success, and the Bateman gradient, which requires knowledge of the genetic mating system. An upper limit on the magnitude of the selection differential on any sexually selected trait is given by the product of the standard deviation in relative mating success and the Bateman gradient. This latter view of the maximum selection differential provides a clearer focus on the important aspects of precopulatory sexual selection than other methods and therefore should be an important part of future studies of sexual selection.

The equilibrium sequence diversity of genes within a population and the rate of sequence divergence between populations or species depends on a variety of factors, including expression pattern, mutation rate, nature of selection, random drift, and mating system. Here, we extend population genetic theory developed for maternal-effect genes to predict the equilibrium polymorphism within species and sequence divergence among species for genes with social effects on fitness. We show how the fitness effects of genes, mating system, and genetic system affect predicted gene polymorphism. We find that, because genes with indirect social effects on fitness effectively experience weaker selection, they are expected to harbor higher levels of polymorphism relative to genes with direct fitness effects. The relative increase in polymorphism is proportional to the inverse of the genetic relatedness between individuals expressing the gene and their social partners that experience the fitness effects of the gene. We find a similar pattern of more rapid divergence between populations or species for genes with indirect social effects relative to genes with direct effects. We focus our discussion on the social insects, organisms with diverse indirect genetic effects, mating and genetic systems, and we suggest specific examples for testing our predictions with emerging sociogenomic tools.

The sensory bias model for the evolution of mating preferences states that mating preferences evolve as correlated responses to selection on nonmating behaviors sharing a common sensory system. The critical assumption is that pleiotropy creates genetic correlations that affect the response to selection. I simulated selection on populations of neural networks to test this. First, I selected for various combinations of foraging and mating preferences. Sensory bias predicts that populations with preferences for like-colored objects (red food and red mates) should evolve more readily than preferences for differently colored objects (red food and blue mates). Here, I found no evidence for sensory bias. The responses to selection on foraging and mating preferences were independent of one another. Second, I selected on foraging preferences alone and asked whether there were correlated responses for increased mating preferences for like-colored mates. Here, I found modest evidence for sensory bias. Selection for a particular foraging preference resulted in increased mating preference for similarly colored mates. However, the correlated responses were small and inconsistent. Selection on foraging preferences alone may affect initial levels of mating preferences, but these correlations did not constrain the joint evolution of foraging and mating preferences in these simulations.

We performed a quantitative trait locus (QTL) analysis of epicuticular hydrocarbon variation in 1650 F₂ males from crosses of Baja California and mainland Mexico populations of Drosophila mojavensis cultured on two major host cacti. Principal component (PC) analysis revealed five PCs that accounted for 82% of the total epicuticular hydrocarbon variation. Courtship trials with mainland females were used to characterize hydrocarbon profiles of mated and unmated F₂ males, and logistic regression analysis showed that cactus substrates, two PCs, and a PC by cactus interaction were associated with mating success. Multiple QTLs were detected for each hydrocarbon PC and seven G × E (cactus) interactions were uncovered for the X, second, and fourth chromosomes. Males from the courtship trials and virgins were used, so “exposure to females” was included as a factor in QTL analyses. “Exposed” males expressed significantly different hydrocarbon profiles than virgins for most QTLs, particularly for the two PCs associated with mating success. Ten QTLs showed G × E (exposure) interactions with most resulting from mainland genotypes expressing altered hydrocarbon amounts when exposed to females compared to Baja genotypes. Many cactus × exposure interaction terms detected across QTL and all PCs confirmed that organ pipe-reared males expressed significantly lower hydrocarbon amounts when exposed to females than when reared on agria cactus. Epicuticular hydrocarbon variation in D. mojavensis is therefore a multigenic trait with some epistasis, multiple QTLs exhibited pleiotropy, correlated groups of hydrocarbons and cactus substrates determined courtship success, and males altered their hydrocarbon profiles in response to females.

Understanding speciation depends on an accurate assessment of the reproductive barriers separating newly diverged populations. In several taxonomic groups, prezygotic barriers, especially preferences for conspecific mates, are thought to play the dominant role in speciation. However, the importance of postzygotic barriers (i.e., low fitness of hybrid offspring) may be widely underestimated. In this study, we examined how well the widely used proxy of postzygotic isolation (reproductive output of F₁ hybrids) reflects the long-term fitness consequences of hybridization between two closely related species of birds. Using 40 species-specific single nucleotide polymorphism (SNP) markers, we genotyped a mixed population of collared and pied flycatchers (Ficedula albicollis and F. hypoleuca) to identify grand- and great grand-offspring from interspecific crosses to derive an accurate, multigeneration estimate of postzygotic isolation. Two independent estimates of fitness show that hybridization results in 2.4% and 2.7% of the number of descendents typical of conspecific pairing. This postzygotic isolation was considerably stronger than estimates based on F₁ hybrids. Our results demonstrate that, in nature, combined selection against hybrids and backcrossed individuals may result in almost complete postzygotic isolation between two comparatively young species. If these findings are general, postzygotic barriers separating hybridizing populations may be much stronger than previously thought.

Divergent selection between contrasting habitats can sometimes drive adaptive divergence and the evolution of reproductive isolation in the face of initially high gene flow. “Progress” along this ecological speciation pathway can range from minimal divergence to full speciation. We examine this variation for threespine stickleback fish that evolved independently across eight lake-stream habitat transitions. By quantifying stickleback diets, we show that lake-stream transitions usually coincide with limnetic-benthic ecotones. By measuring genetically based phenotypes, we show that these ecotones often generate adaptive divergence in foraging morphology. By analyzing neutral genetic markers (microsatellites), we show that adaptive divergence is often associated with the presence of two populations maintaining at least partial reproductive isolation in parapatry. Coalescent-based simulations further suggest that these populations have diverged with gene flow within a few thousand generations, although we cannot rule out the possibility of phases of allopatric divergence. Finally, we find striking variation among the eight lake-stream transitions in progress toward ecological speciation. This variation allows us to hypothesize that progress is generally promoted by strong divergent selection and limited dispersal across the habitat transitions. Our study thus makes a case for ecological speciation in a parapatric context, while also highlighting variation in the outcome.

Speciation via interspecific hybrids is very rare in animals, as compared to plants. Whereas most plants overcome the problem of meiosis between different chromosome sets by tetraploidization, animal hybrids often escape hybrid sterility by clonal reproduction. This comes at the expense of genetic diversity and the ability to purge deleterious mutations. However, here we show that all-hybrid populations of diploid (LR) and triploid (LLR and LRR) water frogs (Pelophylax esculentus) have secondarily acquired sexual reproduction. First, in a crossing experiment analyzed with microsatellite markers, triploid hybrids of both sexes and genotypes (LLR and LRR) recombined their homospecific genomes. Second, the great majority of natural populations investigated had low multilocus linkage disequilibrium, indicating a high recombination rate. As predicted from mating system models, the L genome had constant, low levels of linkage disequilibrium, whereas linkage disequilibrium in the R genome showed a significant reduction with increasing proportion of recombining triploids. This direct evidence of sexual reproduction in P. esculentus calls for a change of the conventional view of hybridogens as clonally reproducing diploids. Rather, hybridogens can be independent sexually reproducing units with an evolutionary potential.

A classic paradigm in evolutionary biology is that geographically isolated clades inhabiting similar selective regimes will diversify to create similar sets of phenotypes in different locations (e.g., similar stickleback species in different lakes, similar Anolis ecomorphs on different islands). Such parallel radiations are not generally expected to occur in sympatry because the available niche space would be filled by whichever clade is diversified first. Here, we document a very different pattern, the parallel evolution of similar body-size morphs in three sympatric clades of plethodontid salamanders (Desmognathus, Plethodon, Spelerpinae) in eastern North America. Using a comprehensive, time-calibrated phytogeny of North American plethodontids from nuclear and mitochondrial DNA sequences, we show that these three clades have undergone replicated patterns of evolution in body size and that this parallel diversification occurred in broad-scale sympatry. At the local scale, we find that coexisting species from these clades are more similar in body size than expected under a null model in which species are randomly assembled into communities. These patterns are particularly surprising in that competition is known to be important in driving phenotypic diversification and limiting local coexistence of similar-sized species within these clades. Although parallel diversification of sympatric clades may seem counterintuitive, we discuss several ecological and evolutionary factors that may allow the phenomenon to occur.

Indirect genetic effects (IGEs), which occur when phenotypic expression in one individual is influenced by genes in another conspecific individual, may have a drastic effect on evolutionary response to selection. General evolutionary models of IGEs have been developed using two distinct theoretical frameworks derived from maternal effects theory. The first framework is trait-based and focuses on how phenotypes are influenced by specific traits in a social partner, with the strength of interactions defined by the matrix Ö. The second framework partitions total genetic variance into components representing direct effects, indirect effects, and the covariance between them, without identifying specific social traits responsible for IGEs. The latter framework has been employed more commonly by empiricists because the methods for estimating variance components are relatively straightforward. Here, we show how these two theoretical frameworks are related to each other and derive equations that can be used to translate between them. This translation leads to a generalized method that can be used to estimate Ψ via standard quantitative genetic breeding designs or pedigrees from natural populations. This method can be used in a very general set of circumstances and is widely applicable to all IGEs, including maternal effects and other interactions among relatives.

How and why cooperation evolves, particularly among nonrelatives, remains a major paradox for evolutionary biologists and behavioral ecologists. Although much attention has focused on fitness consequences associated with cooperating, relatively little is known about the second component of evolutionary change, the inheritance of cooperation or reciprocity. The genetics of behaviors that can only be expressed in the context of interactions are particularly difficult to describe because the relevant genes reside in multiple social partners. Indirect genetic effects (IGEs) describe the influence of genes carried in social partners on the phenotype of a focal individual and thus provide a novel approach to quantifying the genetics underlying interactions such as reciprocal cooperation. We used inbred lines of guppies and a novel application of IGE theory to describe the dual genetic control of predator inspection and social behavior, both classic models of reciprocity. We identified effects of focal strain, social group strain, and interactions between focal and group strains on variation in focal behavior. We measured ψ;, the coefficient of the interaction, which describes the degree to which an individuals phenotype is influenced by the phenotype of its social partners. The genetic identity of social partners substantially influences inspection behavior, measures of threat assessment, and schooling and does so in positively reinforcing manner. We therefore demonstrate strong IGEs for antipredator behavior that represent the genetic variation necessary for the evolution of reciprocity.

Despite abundant empirical evidence that inbreeding depression varies with both the environment and the genotypic context, theoretical predictions about such effects are still rare. Using a quantitative genetics model, we predict amounts of inbreeding depression for fitness emerging from Gaussian stabilizing selection on some phenotypic trait, on which, for simplicity, genetic effects are strictly additive. Given the strength of stabilizing selection, inbreeding depression then varies simply with the genetic variance for the trait under selection and the distance between the mean breeding value and the optimal phenotype. This allows us to relate the expected inbreeding depression to the degree of maladaptation of the population to its environment. We confront analytical predictions with simulations, in well-adapted populations at equilibrium, as well as in maladapted populations undergoing either a transient environmental shift, or gene swamping in heterogeneous habitats. We predict minimal inbreeding depression in situations of extreme maladaptation. Our model provides a new basis for interpreting experiments that measure inbreeding depression for the same set of genotypes in different environments, by demonstrating that the history of adaptation, in addition to environmental harshness per se, may account for differences in inbreeding depression.

Flower shape has evolved in most plants as a consequence of pollinator-mediated selection. Unfortunately, no study has explored the genetic variation of flower shape, despite that this information is crucial to understand its adaptive evolution. Our main goal here is to determine heritability of corolla shape in Erysimum mediohispanicum (Brassicaceae). Also, we explore heritability of other pollinator-selected traits in this plant species, such as plant size, flower display, and corolla size. In addition, we investigate genetic correlations between all these traits. We found significant heritability for one plant-size trait (stalk height), for number of flowers, for all corolla-size traits (corolla diameter, corolla tube length and corolla tube width), and for corolla shape. Consequently, this species retains a high ability to respond to the selection exerted by its pollinators. Genetic correlation was strong between all functionally related traits and between flower number and plant size, weak between corolla size and plant size and no correlation between corolla shape and any other trait. Thus, selection affecting some E. mediohispanicum traits would also indirectly affect other functionally related and unrelated traits. More importantly, the observed genetic correlation seems to be at least partially adaptive because positive correlational selection currently acts on the covariance between some of these traits (Gómez 2003; Gómez et al. 2006).

Developmental instability (DI), as measured by fluctuating asymmetry (FA), may reflect fitness and facilitate the expression of morphological variation. Insights in the underlying mechanisms and magnitude of DI during early development would increase our understanding of its role in evolutionary biology. We studied associations between FA and congenital abnormalities of different origins and functional systems in deceased human fetuses. Major congenital abnormalities corresponded to severe, often-lethal developmental disorders disrupting normal development from early organogenesis onward, but only moderately increased FA. Lower FA with age also supported the hypothesis that more severe abnormalities, leading to an earlier death, increased DI. Although FA related significantly to measures of fitness or health, we anticipated stronger associations because fetal health problems were detrimental. Furthermore, elevated FA occurred in only 4 of 17 disorders (left—right patterning, limb defects, and problems of bronchopulmonary and urogenital system). Fetuses experiencing major abnormalities other than these four types did not show increased FA. This suggests that the functional importance of symmetry in limbs has resulted in strong selection for symmetry and reduced its sensitivity to stress. Finally, the observed patterns suggest that specific developmental pathways have a stronger effect on DI than others do.

The term “differential dominance” describes the situation in which the dominance effects at a pleiotropic locus vary between traits. Directional selection on the phenotype can lead to balancing selection on differentially dominant pleiotropic loci. Even without any individual overdominant traits, some linear combination of traits will display overdominance at a locus displaying differential dominance. Multivariate overdominance may be responsible, in part, for high levels of heterozygosity found in natural populations. We examine differential dominance of 70 mouse skeletal traits at 92 quantitative trait loci (QTL). Our results indicate moderate to strong additive and dominance effects at pleiotropic loci, low levels of individual-trait overdominance, and universal multivariate overdominance. Multivariate overdominance affects a range of 6% to 81% of morphospace, with a mean of 32%. Multivariate overdominance tends to affect a larger percentage of morphospace at pleiotropic loci with antagonistic effects on multiple traits (42%). We conclude that multivariate overdominance is common and should be considered in models and in empirical studies of the role of genetic variation in evolvability.

The ability of some bacteria to take up and recombine DNA from the environment is an important evolutionary problem because its function is controversial; although populations may benefit in the long-term from the introduction of new alleles, cells also reap immediate benefits from the contribution of DNA to metabolism. To clarify how selection has acted, we have characterized competence in natural isolates of H. influenzae by measuring DNA uptake and transformation. Most of the 34 strains we tested became competent, but the amounts of DNA they took up and recombined varied more than 1000-fold. Differences in recombination were not due to sequence divergence and were only partly explained by differences in the amounts of DNA taken up. One strain was highly competent during log phase growth, unlike the reference strain Rd, but several strains did not develop competence under any of the tested conditions. Analysis of competence genes identified genetic defects in two poorly transformable strains. These results show that strains can differ considerably in the amount of DNA they take up and recombine, indicating that the benefit associated with competence is likely to vary in space and/or time.

Rising temperatures associated with global warming present a challenge to the fate of many aquatic organisms. Although rapid evolutionary response to temperature-mediated selection may allow local persistence of populations under global warming, and therefore is a key aspect of evolutionary biology, solid proof of its occurrence is rare. In this study, we tested for genetic adaptation to an increase in temperature in the water flea Daphnia magna, a keystone species in freshwater systems, by performing a thermal selection experiment under laboratory conditions followed by the quantification of microevolutionary responses to temperature for both life-history traits as well as for intraspecific competitive strength. After three months of selection, we found a microevolutionary response to temperature in performance, but only in one of two culling regimes, highlighting the importance of population dynamics in driving microevolutionary change within populations. Furthermore, there was an evolutionary increase in thermal plasticity in performance. The results of the competition experiment were in agreement with predictions based on performance as quantified in the life table experiment and illustrate that microevolution within a short time frame has the ability to influence the outcome of intraspecific competition.

Many plants, insects, and crustaceans show within-population variability in dormancy length. The question of whether such variability corresponds to a genetic polymorphism of pure strategies or a mixed bet-hedging strategy, and how the level of phenotypic variability can evolve remain unknown for most species. Using an eco-genetic model rooted in a 25-year ecological field study of a Chestnut weevil, Curculio elephas, we show that its diapause-duration variability is more likely to have evolved by the spread of a bet-hedging strategy than by the establishment of a genetic polymorphism. Investigating further the adaptive dynamics of diapause-duration variability, we find two unanticipated patterns of general interest. First, there is a trade-off between the ability of bet-hedging strategies to persist on an ecological time scale and their ability to invade. The optimal strategy (in terms of persistence) cannot invade, whereas suboptimal bet-hedgers are good invaders. Second, we describe an original evolutionary dynamics where each bet-hedging strategy (defined by its rate of prolonged diapause) resists invasion by all others, so that the first type of bet-hedger to appear persists on an evolutionary time scale. Such “evolutionary priority effect” could drive the evolution of maladapted levels of diapause-duration variability.

The Red Queen coevolutionary hypothesis predicts that parasites drive oscillations in host genotype frequencies due to frequencydependent selection where common hosts are at disadvantage. However, examples of this phenomenon in natural populations are scarce. To examine if the Red Queen theory operates in the wild, we studied the genetic structure of populations of the crustacean waterflea (Daphnia), in relation to their infection levels, for which we collected multiple samples from a variety of lakes. The most common clone in a given population was often underinfected. This advantage, however, did not remain stable over time. Instead, the most common clone decreased in frequency over subsequent generations, indicating that parasites can track common clones. Such decreases were not observed in uninfected populations. Moreover, host clonal evenness was higher across the set of infected lakes compared to uninfected lakes; suggesting that any common clone is selected against when parasites are present. These results strongly suggest that Red Queen dynamics do operate in the wild.

Adaptive population divergence is often driven by divergent natural selection, but can be constrained by the homogenizing effect of gene flow between populations. Indeed, a common pattern in nature is an inverse correlation between the degree of adaptive phenotypic divergence between populations and levels of gene flow between populations. However, there is essentially no experimental data on whether this correlation arises because gene flow constrains adaptation or, conversely, because adaptive divergence causes barriers to gene flow (ecological speciation). Here, I report increased adaptive divergence in cryptic color pattern between a pair of Timema insect populations following an experimental reduction in between-population gene flow. The reduction in gene flow arose due to a natural experiment, and thus was not replicated at a second site. However, temporal replication of the trends among six generations of data, coupled with a lack of increased adaptive divergence for two other population pairs where gene flow was not manipulated (i.e., control sites), argues that the results did not arise by chance. Estimates of dispersal ability and population size further support reduced gene flow, rather than increased genetic drift, as the cause of divergence. Thus, the findings provide experimental evidence that gene flow constrains adaptation in nature.

Reciprocity is often invoked to explain cooperation. Reciprocity is cognitively demanding, and both direct and indirect reciprocity require that individuals store information about the propensity of their partners to cooperate. By contrast, generalized reciprocity, wherein individuals help on the condition that they received help previously, only relies on whether an individual received help in a previous encounter. Such anonymous information makes generalized reciprocity hard to evolve in a well-mixed population, as the strategy will lose out to pure defectors. Here we analyze a model for the evolution of generalized reciprocity, incorporating assortment of encounters, to investigate the conditions under which it will evolve. We show that, in a well-mixed population, generalized reciprocity cannot evolve. However, incorporating assortment of encounters can favor the evolution of generalized reciprocity in which indiscriminate cooperation and defection are both unstable. We show that generalized reciprocity can evolve under both the prisoner's dilemma and the snowdrift game.

Experimental evolution, particularly experimental sexual selection in which sexual selection strength is manipulated by altering the mating system, is an increasingly popular method for testing evolutionary theory. Concerns have arisen regarding genetic diversity variation across experimental treatments: differences in the number and sex ratio of breeders (effective population size; N_e) and the potential for genetic hitchhiking, both of which may cause different levels of genetic variation between treatments. Such differences may affect the selection response and confound interpretation of results. Here we use both census-based estimators and molecular marker-based estimates to empirically test how experimental evolution of sexual selection in Drosophila pseudoobscura impacts N_e and autosomal genetic diversity. We also consider effects of treatment on X-linked N_es, which have previously been ignored. Molecular autosomal marker-based estimators indicate that neither N_e nor genetic diversity differs between treatments experiencing different sexual selection intensities; thus observed evolutionary responses reflect selection rather than any confounding effects of experimental design. Given the increasing number of studies on experimental sexual selection, we also review the census N_es of other experimental systems, calculate X-linked N_e, and compare how different studies have dealt with the issues of inbreeding, genetic drift, and genetic hitchhiking to help inform future designs.

Belief in creationism and intelligent design is widespread and gaining significance in a number of countries. This article examines the characteristics of science and of religions and the possible relationship between science and religion. I argue that creationism is sometimes best seen not as a misconception but as a worldview. In such instances, the most to which a science educator (whether in school, college or university) can normally aspire is to ensure that students with creationist beliefs understand the scientific position. In the short term, the scientific worldview is unlikely to supplant a creationist one for students who are firm creationists. We can help students to find their evolutionary biology courses interesting and intellectually challenging without their being threatening. Effective teaching in this area can help students not only learn about the theory of evolution but better appreciate the way science is done, the procedures by which scientific knowledge accumulates, the limitations of science, and the ways in which scientific knowledge differs from other forms of knowledge.