EVOLUTION

Since 1983, study of natural selection has relied heavily on multiple regression of fitness on the values for a set of traits via ordinary least squares (OLSs), as proposed by Lande and Arnold, to obtain an estimate of the quadratic relationship between fitness and the traits, the fitness surface. However, well-known statistical problems with this approach can affect inferences about selection. One key concern is that measures of lifetime fitness do not conform to a normal or any other standard sampling distribution, as needed to justify the usual statistical tests. Another is that OLS may yield an estimate of the sign of the fitness function's curvature that is opposite to the truth. We here show that the recently developed aster modeling approach, which explicitly models the components of fitness as the basis for inferences about lifetime fitness, eliminates these problems. We illustrate selection analysis via aster using simulated datasets involving five fitness components expressed in each of four years. We demonstrate that aster analysis yields accurate estimates of the fitness function in cases in which OLS misleads, as well as accurate confidence regions for directional selection gradients. Further, to evaluate selection when many traits are under consideration, we recommend model selection by information criteria and frequentist model averaging.

Thermal adaptation to spatially varying environmental conditions occurs in a wide range of species, but what is less clear is the nature of fitness trade-offs associated with this temperature adaptation. Here, populations of the intertidal copepod Tigriopus californicus are examined at both local and latitudinal scales to determine whether these populations have evolved differences in their survival under high temperature stress. A clear pattern of increasing high temperature stress tolerance is seen with decreasing latitude, consistent with temperature adaptation. Additionally, there is also evidence for significant variation in thermal tolerance on a smaller scale. The competitive fitness of pairs of northern and southern copepod populations were also examined under a series of lower, more moderate temperatures. These fitness assays show that the southern populations that have the best survival under extreme high temperatures have lowered competitive fitness at the lower temperatures tested, whereas the fitness of the southern populations exceeded that of the northern populations at the highest temperatures tested. Combined, these results suggest that there may be evolutionary trade-offs between performance at high and stressful temperatures and fitness at moderate temperatures in this species.

The genic capture model offers a promising solution to the lek paradox. Heightened condition dependency of sexually selected traits is a prerequisite of this model. Condition dependency is empirically inferred by the sensitivity of traits to stressors. The magnitude of ecological stress (e.g., competition and predation) experienced by populations varies considerably. Thus, condition dependence should manifest more in populations experiencing higher levels of stress. We experimentally assessed the sensitivity of a sexually selected trait (posterior gnathopod) to food resource stress in an amphipod species. We found that gnathopod size variation was 59% higher under food stress, with no corresponding effect on nonsexually selected traits. In addition, we assessed levels of gnathopod variation and the allometry of gnathopods for males sampled from natural populations for two amphipod species that experience different levels of stress (driven by contrasting size-selective predation and associated life-history trade-offs). Populations that experience higher resource stress had both steeper allometries and greater gnathopod size variation. These results suggest that the magnitude of ecological stress experienced by natural populations strongly impacts condition dependency of sexually selected traits, and could play an important role in shaping trait variation and thus the opportunity for sexual selection.

Despite the directional selection acting on life-history traits, substantial amounts of standing variation for these traits have frequently been found. This variation may result from balancing selection (e.g., through genetic trade-offs) or from mutation-selection balance. These mechanisms affect allele frequencies in different ways: Under balancing selection alleles are maintained at intermediate frequencies, whereas under mutation-selection balance variation is generated by deleterious mutations and removed by directional selection, which leads to asymmetry in the distribution of allele frequencies. To investigate the importance of these two mechanisms in maintaining heritable variation in oviposition rate of the two-spotted spider mite, we analyzed the response to artificial selection. In three replicate experiments, we selected for higher and lower oviposition rate, compared to control lines. A response to selection only occurred in the downward direction. Selection for lower oviposition rate did not lead to an increase in any other component of fitness, but led to a decline in female juvenile survival. The results suggest standing variation for oviposition rate in this population consists largely of deleterious alleles, as in a mutation-selection balance. Consequently, the standing variation for this trait does not appear to be indicative of its adaptive potential.

Interactions among conspecifics influence social evolution through two distinct but intimately related paths. First, they provide the opportunity for indirect genetic effects (IGEs), where genes expressed in one individual influence the expression of traits in others. Second, interactions can generate social selection when traits expressed in one individual influence the fitness of others. Here, we present a quantitative genetic model of multivariate trait evolution that integrates the effects of both IGEs and social selection, which have previously been modeled independently. We show that social selection affects evolutionary change whenever the breeding value of one individual covaries with the phenotype of its social partners. This covariance can be created by both relatedness and IGEs, which are shown to have parallel roles in determining evolutionary response. We show that social selection is central to the estimation of inclusive fitness and derive a version of Hamilton's rule showing the symmetrical effects of relatedness and IGEs on the evolution of altruism. We illustrate the utility of our approach using altruism, greenbeards, aggression, and weapons as examples. Our model provides a general predictive equation for the evolution of social phenotypes that encompasses specific cases such as kin selection and reciprocity. The parameters can be measured empirically, and we emphasize the importance of considering both IGEs and social selection, in addition to relatedness, when testing hypotheses about social evolution.

Social-learner-explorer (SE) is a learning strategy that combines accurate social learning with exploratory individual learning in that order. Arguably, it is one of the few plausible learning strategies that can support cumulative culture. We investigate numerically the factors that affect the evolution of SE in an environmentally heterogeneous two-island model. Conditions favorable to the evolution of SE include a small exogenous cost of social learning, the occurrence of migration after social learning but before individual learning, the ability to adaptively modify the behavioral phenotype in the postmigration environment (asymmetrical individual learning), and a relatively high migration rate. The implications of our model for the evolution of SE in humans are discussed. Of particular interest is the prediction that behaviors affecting fitness would have to be socially learned in the natal environment and then subsequently modified by individual learning in the postmigration environment, suggesting a life-cycle stage dependent reliance on the two types of learning.

What are imprinted genes doing in the adult brain? Genomic imprinting is when a gene's expression depends upon parent of origin. According to the prevailing view, the “kinship theory” of genomic imprinting, this effect is driven by evolutionary conflicts between genes inherited via sperm versus egg. This theory emphasizes conflicts over the allocation of maternal resources, and focuses upon genes that are expressed in the placenta and infant brain. However, there is growing evidence that imprinted genes are also expressed in the juvenile and adult brain, after cessation of parental care. These genes have recently been suggested to underpin neurological disorders of the social brain such as psychosis and autism. Here we advance the kinship theory by developing an evolutionary model of genomic imprinting for social behavior beyond the nuclear family. We consider the role of demography and mating system, emphasizing the importance of sex differences in dispersal and variance in reproductive success. We predict that, in hominids and birds, altruism will be promoted by paternally inherited genes and egoism will be promoted by maternally inherited genes. In nonhominid mammals we predict more diversity, with some mammals showing the same pattern and other showing the reverse. We discuss the implications for the evolution of psychotic and autistic spectrum disorders in human populations with different social structures.

Understanding the reasons why different parasites cause different degrees of harm to their hosts is an important objective in evolutionary biology. One group of models predicts that if hosts are infected with more than one strain or species of parasite, then competition between the parasites will select for higher virulence. While this idea makes intuitive sense, empirical data to support it are rare and equivocal. We investigated the relationship between fitness and virulence during both inter- and intraspecific competition for a fungal parasite of insects, Metarhizium anisopliae. Contrary to theoretical expectations, competition favored parasite strains with either a lower or a higher virulence depending on the competitor: when in interspecific competition with an entomopathogenic nematode, Steinernema feltiae, less virulent strains of the fungus were more successful, but when competing against conspecific fungi, more virulent strains were better competitors. We suggest that the nature of competition (direct via toxin production when competing against the nematode, indirect via exploitation of the host when competing against conspecific fungal strains) determines the relationship between virulence and competitive ability.

Vector-borne microbes necessarily co-occur with their hosts and vectors, but the degree to which they share common evolutionary or biogeographic histories remains unexplored. We examine the congruity of the evolutionary and biogeographic histories of the bacterium and vector of the Lyme disease system, the most prevalent vector-borne disease in North America. In the eastern and midwestern US, Ixodes scapularis ticks are the primary vectors of Borrelia burgdorferi, the bacterium that causes Lyme disease. Our phylogeographic and demographic analyses of the 16S mitochondrial rDNA suggest that northern I. scapularis populations originated from very few migrants from the southeastern US that expanded rapidly in the Northeast and subsequently in the Midwest after the recession of the Pleistocene ice sheets. Despite this historical gene flow, current tick migration is restricted even between proximal sites within regions. In contrast, B. burgdorferi suffers no barriers to gene flow within the northeastern and midwestern regions but shows clear interregional migration barriers. Despite the intimate association of B. burgdorferi and I. scapularis, the population structure, evolutionary history, and historical biogeography of the pathogen are all contrary to its arthropod vector. In the case of Lyme disease, movements of infected vertebrate hosts may play a larger role in the contemporary expansion and homogenization of the pathogen than the movement of tick vectors whose populations continue to bear the historical signature of climate-induced range shifts.

Organisms from prokaryotes to plants and animals make costly investments in diffusible beneficial external products. While the costs of producing such products are born only by the producer, the benefits may be distributed more widely. How are external goods-producing populations stabilized against invasion by nonproducing variants that receive the benefits without paying the cost? This question parallels the classic question of altruism, but because external goods production need not be altruistic per se, a broader range of conditions may lead to the maintenance of these traits. We start from the physics of diffusion to develop an expression for the conditions that favor the production of diffusible external goods. Important variables in determining the evolutionary outcome include the diffusion coefficient of the good, the distance between individuals, and the uptake rate of the external good. These variables join the coefficient of relatedness and the cost/benefit ratio in an expanded form of Hamilton's rule that includes both selfish and altruistic paths to the evolution of external goods strategies. This expanded framework can be applied to any external goods trait, and is a useful heuristic even when it is difficult to quantify the fitness consequences of producing the good.

Robust estimates of dispersal are critical for understanding population dynamics and local adaptation, as well as for successful spatial management. Genetic isolation by distance patterns hold clues to dispersal, but understanding these patterns quantitatively has been complicated by uncertainty in effective density. In this study, we genotyped populations of a coral reef fish (Amphiprion clarkii) at 13 microsatellite loci to uncover fine-scale isolation by distance patterns in two replicate transects. Temporal changes in allele frequencies between generations suggested that effective densities in these populations are 4–21 adults/km. A separate estimate from census densities suggested that effective densities may be as high as 82–178 adults/km. Applying these effective densities with isolation by distance theory suggested that larval dispersal kernels in A. clarkii had a spread near 11 km (4–27 km). These kernels predicted low fractions of self-recruitment in continuous habitats, but the same kernels were consistent with previously reported, high self-recruitment fractions (40–60%) when realistic levels of habitat patchiness were considered. Our results suggested that ecologically relevant larval dispersal can be estimated with widely available genetic methods when effective density is measured carefully through cohort sampling and ecological censuses, and that self-recruitment studies should be interpreted in light of habitat patchiness.

By measuring the direct and indirect fitness costs and benefits of sexual interactions, the feasibility of alternate explanations for polyandry can be experimentally assessed. This approach becomes more complicated when the relative magnitude of the costs and/or benefits associated with multiple mating (i.e., remating with different males) vary with female condition, as this may influence the strength and direction of sexual selection. Here, using the model organism Drosophila melanogaster, we test whether the indirect benefits that a nonvirgin female gains by remating (“trading-up”) are influenced by her condition (body size). We found that remating by small-bodied, low-fecundity females resulted in the production of daughters of relatively higher fecundity, whereas the opposite pattern was observed for large-bodied females. In contrast, remating had no measurable effect on the relative reproductive success of sons from dams of either body size. These results are consistent with a hypothesis based on sexually antagonistic genetic variation. The implications of these results to our understanding of the evolution and consequences of polyandry are discussed.

Molecular rate heterogeneity, whereby rates of molecular evolution vary among groups of organisms, is a well-documented phenomenon. Nonetheless, its causes are poorly understood. For animals, generation time is frequently cited because longer-lived species tend to have slower rates of molecular evolution than their shorter-lived counterparts. Although a similar pattern has been uncovered in flowering plants, using proxies such as growth form, the underlying process has remained elusive. Here, we find a deceleration of molecular evolutionary rate to be coupled with the origin of arborescence in ferns. Phylogenetic branch lengths within the “tree fern” clade are considerably shorter than those of closely related lineages, and our analyses demonstrate that this is due to a significant difference in molecular evolutionary rate. Reconstructions reveal that an abrupt rate deceleration coincided with the evolution of the long-lived tree-like habit at the base of the tree fern clade. This suggests that a generation time effect may well be ubiquitous across the green tree of life, and that the search for a responsible mechanism must focus on characteristics shared by all vascular plants. Discriminating among the possibilities will require contributions from various biological disciplines, but will be necessary for a full appreciation of molecular evolution.

A key question in sexual selection is whether the ability of males to fertilize eggs under sperm competition exhibits heritable genetic variation. Addressing this question poses a significant problem, however, because a male's ability to win fertilizations ultimately depends on the competitive ability of rival males. Attempts to partition genetic variance in sperm competitiveness, as estimated from measures of fertilization success, must therefore account for stochastic effects due to the random sampling of rival sperm competitors. In this contribution we suggest a practical solution to this problem. We advocate the use of simple cross-classified breeding designs for partitioning sources of genetic variance in sperm competitiveness and fertilization success and show how these designs can be used to avoid stochastic effects due to the random sampling of rival sperm competitors. We illustrate the utility of these approaches by simulating various scenarios for estimating genetic parameters in sperm competiveness, and show that the probability of detecting additive genetic variance in this trait is restored when stochastic effects due to the random sampling of rival sperm competitors are controlled. Our findings have important implications for the study of the evolutionary maintenance of polyandry.

The telencephalon is proportionately larger in parrots than in galliformes (chicken-like birds), whereas the midbrain tectum is proportionately smaller. We here test the hypothesis that the adult species difference in midbrain proportion is due to an evolutionary change in early brain patterning. In particular, we compare the size of the early embryonic midbrain between parakeets (Melopsittacus undulatus) and bobwhite quail (Colinus virgianus) by examining the expression domains of transcription factors Pax6 and Gbx2, which are expressed in the forebrain and hindbrain, respectively. Because these expression domains form rostral and caudal borders with the presumptive midbrain when this region is specified (Hamburger-Hamilton stages 9–11), they allow us to measure and compare the sizes of a molecularly defined presumptive midbrain in the two species. Based on published data from older embryos, we predicted that the molecularly defined midbrain territory is significantly larger in quail than parakeets. Indeed, our data show that normalized midbrain length is 33% greater in quail and that the midbrain to forebrain ratio is 28% greater. This is strong evidence of a significant species difference in early brain patterning.

A broad understanding of multimodal courtship function necessitates knowledge of the potential information content of signal components, the efficacy of signal components in eliciting the appropriate receiver response, and the fitness consequences of mating decisions based upon various signal components. We present data addressing each of these requirements for the multimodal-signaling wolf spider, Schizocosa floridana Bryant. Using diet manipulations, we first demonstrate that both visual and seismic courtship signals are condition-dependent. Next, using high and low-quantity diet individuals in mate choice trials across manipulated signaling environments, we demonstrate that the seismic signal is crucial for mating success and further show that female choosiness is environment-dependent. Females mated more with high diet males only in the absence of visual signals, showing no discrimination in the presence of visual signals. Finally, by quantifying the number of offspring produced by our mated females, we reveal that a female's mating environment, in conjunction with her potential resource availability, influences her fitness – in environments in which females exerted choice, heavier females produced more offspring. Together, this comprehensive set of experiments demonstrates that female choosiness varies across environments, leading to direct fitness consequences.

Divergence in male mating signals and associated female preferences is often an important step in the process of speciation. Reproductive character displacement, the pattern of greater divergence of male signals and/or female preference in sympatry than in allopatry, has been observed in a variety of taxa with different degrees of postzygotic isolation. A number of selective processes, including reinforcement, have been proposed to cause such a pattern. Cases where reproductive character displacement occurs among intraspecific variants are especially informative for understanding how selection acting within a species can lead to the evolution of reproductive barriers and speciation. This study tested the hypothesis that female strawberry poison dart frogs (Dendrobates pumilio) in polymorphic populations of the Bocas del Toro archipelago of Panama show stronger mating discrimination than do females from monomorphic populations, exhibiting an intraspecific pattern of reproductive character displacement. Our results contribute important insights into understanding selection's role in generating the striking diversity of Bocas del Toro's D. pumilio and provide a snapshot of what could be the early stages of reproductive isolation and speciation.

The handicap hypothesis proposes that male signals provide reliable information to females because only males of high condition provide high quality mating benefits and can afford the costs of producing attractive signals. In the context of direct benefits, the handicap hypothesis predicts that benefit quality and signal attractiveness will positively covary among genotypes, positively covary among environments, or be affected by congruent genotype-environment interactions. The latter should occur if the relative condition of a genotype is environment-dependent. We tested these predictions in the variable field cricket, Gryllus lineaticeps. An interaction between male family and nutritional environment affected the expression of a costly signal preferred by females, while only male family affected direct benefit quality. These non-congruent effects of family and nutritional environment are inconsistent with the handicap hypothesis, and appear to have resulted from variation among nutritional environments in the relationship between signal attractiveness and benefit quality. Surprisingly, signal attractiveness was positively correlated with benefit quality when males experienced a low nutrition environment but negatively correlated with benefit quality when males experienced a high nutrition environment. As a result, female choice for direct benefits may be difficult, particularly in heterogeneous environments, unless females can assess the environmental histories of males.

Gene flow is often considered to be one of the main factors that that constrains local adaptation in a heterogeneous environment. However, gene flow may also lead to the evolution of phenotypic plasticity. We investigated the effect of gene flow on local adaptation and phenotypic plasticity in development time in island populations of the common frog Rana temporaria which breed in pools that differ in drying regimes. This was done by investigating associations between traits (measured in a common garden experiment) and selective factors (pool drying regimes and gene flow from other populations inhabiting different environments) by regression analyses and by comparing pairwise FST values (obtained from microsatellite analyses) with pairwise QST values. We found that the degree of phenotypic plasticity was positively correlated with gene flow from other populations inhabiting different environments (among-island environmental heterogeneity), as well as with local environmental heterogeneity within each population. Furthermore, local adaptation, manifested in the correlation between development time and the degree of pool drying on the islands, appears to have been caused by divergent selection pressures. The local adaptation in development time and phenotypic plasticity is quite remarkable, since the populations are young (less than 300 generations) and substantial gene flow is present among islands.

Bacteria frequently exhibit cooperative behaviours but cooperative strains are vulnerable to invasion by cheater strains which reap the benefits of cooperation but do not perform the cooperative behaviour themselves. Bacterial genomes often contain mobile genetic elements such as plasmids. When a gene for cooperative behaviour exists on a plasmid, cheaters can be forced to cooperate by infection with this plasmid, rescuing cooperation in a population where mutation or migration has allowed cheaters to arise. Here we introduce a second plasmid which does not code for cooperation and show that the social dilemma repeats itself at the plasmid level in both within-patch and metapopulation scenarios, and under various scenarios of plasmid incompatibility. Our results suggest that while plasmid carriage of cooperative genes can provide a transient defence against defection in structured environments, plasmid and chromosomal defection remain the only stable strategies in an unstructured environment. We discuss our results in the light of recent bioinformatic evidence that cooperative genes are over-represented on mobile elements.