Nectar robbers influence the trait–fitness relationship of Primula secundiflora

• The trait–fitness relationship influences the strength and direction of floral evolution. To fully understand and predict the evolutionary trajectories of floral traits, it is critical to disentangle the direct and indirect effects of floral traits on plant fitness in natural populations.
• We experimentally quantified phenotypic selection on floral traits through female fitness and estimated the casual effects of nectar robbing with different nectar robbing intensities on trait–fitness relationships in both the L‐ (long‐style and short‐anther phenotype) and S‐morph (short‐style and long‐anther phenotype) flowers among Primula secundiflora populations.
• A larger number of flowers and wider corolla tubes had both direct and indirect positive effects on female fitness in the P. secundiflora populations. The indirect effects of these two traits on female fitness were mediated by nectar robbers. The indirect effect of the number of flowers on female fitness increased with increasing nectar robbing intensity. In most populations, the direct and/or indirect effects of floral traits on female fitness were stronger in the S‐morph flowers than in the L‐morph flowers. In addition, nectar robbers had a direct positive effect on female fitness, but this effect varied between the L‐ and S‐morph flowers.
• These results show the potential role of nectar robbers in influencing the trait–fitness relationships in this primrose species.

     

The fitness threshold model: Random environmental change alters adaptive landscapes

We used a probabilistic optimization model to explore the joint evolutionary effects of random phenotypic and environmental variation. Two forms of environmental noise were defined in which the optimal phenotype remained constant but all organisms experienced either the same proportionate or the same absolute fitness gains and losses. There was no evolutionary effect of proportionate fitness fluctuations. In contrast, the optimal genotype varied with absolute fitness fluctuations, despite the environmental effect being phenotype-independent. We refer to such phenotype-independent fluctuation in absolute fitness as the fitness threshold model, because shared fitness effects determine the zero-fitness points (i.e. the baseline) on an intrinsic fitness function. Thus, environmental effects that are unrelated to a focal trait can cause peak shifts in the genetic optimum for the trait. Changes in the fitness threshold not only changed peak locations, but also altered the slopes defining the peaks, and so should alter the rate of evolution towards optima. This model pertains to evolution in any system, unless there is no phenotypic or environmental variance, or the selection function and distribution of phenotypic error assume similar shapes. Our results have many basic and applied implications for topics such as the maintenance of genetic variation, the canalization of development and the management of natural populations.     

An evolutionary analysis of the relationship between spite and altruism

We investigate the selective pressures on a social trait when evolution occurs in a population of constant size. We show that any social trait that is spiteful simultaneously qualifies as altruistic. In other words, any trait that reduces the fitness of less related individuals necessarily increases that of related ones. Our analysis demonstrates that the distinction between "Hamiltonian spite" and "Wilsonian spite" is not justified on the basis of fitness effects. We illustrate this general result with an explicit model for the evolution of a social act that reduces the recipient's survival ("harming trait"). This model shows that the evolution of harming is favoured if local demes are of small size and migration is low (philopatry). Further, deme size and migration rate determine whether harming evolves as a selfish strategy by increasing the fitness of the actor, or as a spiteful/altruistic strategy through its positive effect on the fitness of close kin.     

Natural selection and quantitative genetics of life-history traits in Western women: a twin study

Whether contemporary human populations are still evolving as a result of natural selection has been hotly debated. For natural selection to cause evolutionary change in a trait, variation in the trait must be correlated with fitness and be genetically heritable and there must be no genetic constraints to evolution. These conditions have rarely been tested in human populations. In this study, data from a large twin cohort were used to assess whether selection will cause a change among women in a contemporary Western population for three life-history traits: age at menarche, age at first reproduction, and age at menopause. We control for temporal variation in fecundity (the "baby boom" phenomenon) and differences between women in educational background and religious affiliation. University-educated women have 35% lower fitness than those with less than seven years education, and Roman Catholic women have about 20% higher fitness than those of other religions. Although these differences were significant, education and religion only accounted for 2% and 1% of variance in fitness, respectively. Using structural equation modeling, we reveal significant genetic influences for all three life-history traits, with heritability estimates of 0.50, 0.23, and 0.45, respectively. However, strong genetic covariation with reproductive fitness could only be demonstrated for age at first reproduction, with much weaker covariation for age at menopause and no significant covariation for age at menarche. Selection may, therefore, lead to the evolution of earlier age at first reproduction in this population. We also estimate substantial heritable variation in fitness itself, with approximately 39% of the variance attributable to additive genetic effects, the remainder consisting of unique environmental effects and small effects from education and religion. We discuss mechanisms that could be maintaining such a high heritability for fitness. Most likely is that selection is now acting on different traits from which it did in pre-industrial human populations.     

Eco-evolutionary vs. habitat contributions to invasion in salmon: experimental evaluation in the wild

Although trait evolution over contemporary timescales is well documented, its influence on ecological dynamics in the wild has received much less attention particularly compared to traditional ecological and environmental factors. For example, evolution over ecologically relevant timescales is expected in populations that colonize new habitats, where it should theoretically enhance fitness, associated vital rates of survival and reproduction, and population growth potential. Nonetheless, success of exotic species is much more commonly attributed to ecological aspects of habitat quality and 'escape from enemies' in the invaded range. Here, we consider contemporary evolution of vital rates in introduced Chinook salmon (Oncorhynchus tshawytscha) that quickly colonized New Zealand and diverged over c. 26 generations. By using experimental translocations, we partitioned the roles of evolution and habitat quality in modifying geographical patterns of vital rates. Variation in habitat quality within the new range had the greatest influence on broad geographical patterns of vital rates, but locally adapted salmon still exhibited more than double the vital rate performance, and hence fitness, of nonlocal counterparts. The scope of this fitness evolution far exceeds the scale of divergence in trait values for these populations, or even the expected fitness effects of particular traits. These results suggest that contemporary evolution can be an important part of the eco-evolutionary dynamics of invasions and highlight the need for studies of the emergent fitness and ecological consequences of such evolution, rather than just changes in trait values.     

The nature of nurture in a wild mammal's fitness

Genetic variation in fitness is required for the adaptive evolution of any trait but natural selection is thought to erode genetic variance in fitness. This paradox has motivated the search for mechanisms that might maintain a population''s adaptive potential. Mothers make many contributions to the attributes of their developing offspring and these maternal effects can influence responses to natural selection if maternal effects are themselves heritable. Maternal genetic effects (MGEs) on fitness might, therefore, represent an underappreciated source of adaptive potential in wild populations. Here we used two decades of data from a pedigreed wild population of North American red squirrels to show that MGEs on offspring fitness increased the population''s evolvability by over two orders of magnitude relative to expectations from direct genetic effects alone. MGEs are predicted to maintain more variation than direct genetic effects in the face of selection, but we also found evidence of maternal effect trade-offs. Mothers that raised high-fitness offspring in one environment raised low-fitness offspring in another environment. Such a fitness trade-off is expected to maintain maternal genetic variation in fitness, which provided additional capacity for adaptive evolution beyond that provided by direct genetic effects on fitness.     

Environmental context drives seed predator-mediated selection on a floral display trait

Linking trait selection to environmental context is necessary to move beyond the simple recognition that selection is spatially variable and to understand what ultimately drives this variation. Natural selection acts through differences among individuals in lifetime fitness and information about effects on fitness components is therefore often not sufficient to gain such an understanding. We investigated how environmental context influenced intensity of seed predation, flower abortion and selection on floral display traits in 44–52 populations of the perennial herb Primula veris over 2 years. Phenotypic selection on both inflorescence height and flower number varied among populations and was mediated partly by pre-dispersal seed predation and flower abortion in one of the years. Among-population variation in selection on inflorescence height, but not flower number, was linked to variation in canopy cover via its effects on seed predation. Lifetime fitness was less sensitive to seed predator damage in shaded environments but estimates of selection based on lifetime fitness agreed qualitatively with those based on seed output. Our results demonstrate that seed predators constitute an important link between environmental conditions and trait evolution in plants, and that selection on plant traits by seed predators can depend on environmental context.     

Evolution of Fitness in Experimental Populations of Vesicular Stomatitis Virus

The evolution of fitness in experimental clonal populations of vesicular stomatitis virus (VSV) has been compared under different genetic (fitness of initial clone) and demographic (population dynamics) regimes. In spite of the high genetic heterogeneity among replicates within experiments, there is a clear effect of population dynamics on the evolution of fitness. Those populations that went through strong periodic bottlenecks showed a decreased fitness in competition experiments with wild type. Conversely, mutant populations that were transferred under the dynamics of continuous population expansions increased their fitness when compared with the same wild type. The magnitude of the observed effect depended on the fitness of the original viral clone. Thus, high fitness clones showed a larger reduction in fitness than low fitness clones under dynamics with included periodic bottleneck. In contrast, the gain in fitness was larger the lower the initial fitness of the viral clone. The quantitative genetic analysis of the trait ``fitness' in the resulting populations shows that genetic variation for the trait is positively correlated with the magnitude of the change in the same trait. The results are interpreted in terms of the operation of MULLER's ratchet and genetic drift as opposed to the appearance of beneficial mutations.     

Intralocus sexual conflict unresolved by sex-limited trait expression

Sexually antagonistic selection generates intralocus sexual conflict, an evolutionary tug-of-war between males and females over optimal trait values [1-4]. Although the potential for this conflict is universal, the evolutionary importance of intralocus conflict is controversial because conflicts are typically thought to be resolvable through the evolution of sex-specific trait development [1-8]. However, whether sex-specific trait expression always resolves intralocus conflict has not been established. We assessed this with beetle populations subjected to bidirectional selection on an exaggerated sexually selected trait, the mandible. Mandibles are only ever developed in males for use in male-male combat, and larger mandibles increase male fitness (fighting [9, 10] and mating success, as we show here). We find that females from populations selected for larger male mandibles have lower fitness, whereas females in small-mandible populations have highest fitness, even though females never develop exaggerated mandibles. This is because mandible development changes genetically correlated characters, resulting in a negative intersexual fitness correlation across these populations, which is the unmistakable signature of intralocus sexual conflict [1]. Our results show that sex-limited trait development need not resolve intralocus sexual conflict, because traits are rarely, if ever, genetically independent of other characters [11]. Hence, intralocus conflict resolution is not as easy as currently thought.     

Costly resistance to parasitism: evidence from simultaneous quantitative trait loci mapping for resistance and fitness in Tribolium castaneum

Information on the molecular basis of resistance and the evolution of resistance is crucial to an understanding of the appearance, spread, and distribution of resistance genes and of the mechanisms of host adaptation in natural populations. One potential important genetic constraint for the evolution of resistance is fitness cost associated with resistance. To determine whether host resistance to parasite infection is associated with fitness costs, we conducted simultaneous quantitative trait loci (QTL) mapping of resistance to parasite infection and fitness traits using the red flour beetle (Tribolium castaneum) and the tapeworm parasite (Hymenolepis diminuta) system in two independent segregating populations. A genome-wide QTL scan using amplified fragment length polymorphism (AFLP) markers revealed three QTL for beetle resistance to tapeworm infection. These three QTL account for 44-58% variance in beetle infection intensity. We identified five QTL for fecundity and five QTL for egg-to-adult viability, which accounted for 36-57% and 36-49%, respectively, of the phenotypic variance in fecundity and egg-to-adult viability. The three QTL conferring resistance were colocalized with the QTL affecting beetle fitness. The genome regions that contain the QTL for parasite resistance explained the majority of the variance in fecundity and egg-to-adult viability in the mapping populations. Colocalization of QTL conferring resistance to parasite infection and beetle fitness may result from the pleiotropic effects of the resistance genes on host fitness or from tight linkages between resistance genes and adverse deleterious mutations. Therefore, our results provide evidence that the genome regions conferring resistance to tapeworm infection are partially responsible for fitness costs in the resistant beetle populations.     

A Pleiotropic Nonadditive Model of Variation in Quantitative Traits

A model of mutation-selection-drift balance incorporating pleiotropic and dominance effects of new mutations on quantitative traits and fitness is investigated and used to predict the amount and nature of genetic variation maintained in segregating populations. The model is based on recent information on the joint distribution of mutant effects on bristle traits and fitness in Drosophila melanogaster from experiments on the accumulation of spontaneous and P element-induced mutations. These experiments suggest a leptokurtic distribution of effects with an intermediate correlation between effects on the trait and fitness. Mutants of large effect tend to be partially recessive while those with smaller effect are on average additive, but apparently with very variable gene action. The model is parameterized with two different sets of information derived from P element insertion and spontaneous mutation data, though the latter are not fully known. They differ in the number of mutations per generation which is assumed to affect the trait. Predictions of the variance maintained for bristle number assuming parameters derived from effects of P element insertions, in which the proportion of mutations with an effect on the trait is small, fit reasonably well with experimental observations. The equilibrium genetic variance is nearly independent of the degree of dominance of new mutations. Heritabilities of between 0.4 and 0.6 are predicted with population sizes from 10(4) to 10(6), and most of the variance for the metric trait in segregating populations is due to a small proportion of mutations (about 1% of the total number) with neutral or nearly neutral effects on fitness and intermediate effects on the trait (0.1-0.5σ(P)). Much of the genetic variance is contributed by recessive or partially recessive mutants, but only a small proportion (about 10%) of the genetic variance is dominance variance. The amount of apparent selection on the trait itself generated by the model is very small. If a model is assumed in which all mutation events have an effect on the quantitative trait, the majority of the genetic variance is contributed by deleterious mutations with tiny effects on the trait. If such a model is assumed for viability, the heritability is about 0.1, independent of the population size.     

Developmental plasticity and the origin of novel forms: unveiling cryptic genetic variation via "use and disuse"

Natural selection eliminates phenotypic variation from populations, generation after generation-an observation that haunted Darwin. So, how does new phenotypic variation arise, and is it always random with respect to fitness? Repeated behavioral responses to a novel environment-particularly those that are learned-are typically advantageous. If those behaviors yield more extreme or novel morphological variants via developmental plasticity, then previously cryptic genetic variation may be exposed to natural selection. Significantly, because the mean phenotypic effect of "use and disuse" is also typically favorable, previously cryptic genetic variation can be transformed into phenotypic variation that is both visible to selection and biased in an adaptive direction. Therefore, use-induced developmental plasticity in a very real sense "creates" new phenotypic variation that is nonrandom with respect to fitness, in contrast to the random phenotypic effects of mutation, recombination, and "direct effects" of environment (stress, nutrition). I offer here (a) a brief review of the immense literature on the effects of "use and disuse" on morphology, (b) a simple yet general model illustrating how cryptic genetic variation may be exposed to selection by developmentally plastic responses that alter trait performance in response to "use and disuse," and (c) a more detailed model of a positive feedback loop between learning (handed behavior) and morphological plasticity (use-induced morphological asymmetry) that may rapidly generate novel phenotypic variation and facilitate the evolution of conspicuous morphological asymmetries. Evidence from several sources suggests that handed behaviors played an important role both in the origin of novel forms (asymmetries) and in their subsequent evolution.     

Overdominance interacts with linkage to determine the rate of adaptation to a new optimum

Overdominance, or a fitness advantage of a heterozygote over both homozygotes, can occur commonly with adaptation to a new optimum phenotype. We model how such overdominant polymorphisms can reduce the evolvability of diploid populations, uncovering a novel form of epistatic constraint on adaptation. The fitness load caused by overdominant polymorphisms can most readily be ameliorated by evolution at tightly linked loci; therefore, traits controlled by multiple loosely linked loci are predicted to be strongly constrained. The degree of constraint is also sensitive to the shape of the relationship between phenotype and fitness, and the constraint caused by overdominance can be strong enough to overcome the effects of clonal interference on the rate of adaptation for a trait. These results point to novel influences on evolvability that are specific to diploids and interact with genetic architecture, and they predict a source of stochastic variability in eukaryotic evolution experiments or cases of rapid evolution in nature.     

The contribution of ancestry,chance, and past and ongoing selection to adaptive evolution

The relative contributions of ancestry, chance, and past and ongoing election to variation in one adaptive (larval feeding rate) and one seemingly nonadaptive (pupation height) trait were determined in populations ofDrosophila melanogaster adapting to either low or high larval densities in the laboratory. Larval feeding rates increased rapidly in response to high density, and the effects of ancestry, past selection and chance were ameliorated by ongoing selection within 15–20 generations. Similarly, in populations previously kept at high larval density, and then switched to low larval density, the decline of larval feeding rate to ancestral levels was rapid (15-20 generations) and complete, providing support for a previously stated hypothesis regarding the costs of faster feeding inDrosophila larvae. Variation among individuals was the major contributor to variation in pupation height, a trait that would superficially appear to be nonadaptive in the environmental context of the populations used in this study because it did not diverge between sets of populations kept at low versus high larval density for many generations. However, the degree of divergence among populations (FST) for pupation height was significantly less than expected for a selectively neutral trait, and we integrate results from previous studies to suggest that the variation for pupation height among populations is constrained by stabilizing selection, with a flat, plateau-like fitness function that, consequently, allows for substantial phenotypic variation within populations. Our results support the view that the genetic imprints of history (ancestry and past selection) in outbreeding sexual populations are typically likely to be transient in the face of ongoing selection and recombination. The results also illustrate the heuristic point that different forms of selection-for example directional versus stabilizing selection—acting on a trait in different populations may often not be due to differently shaped fitness functions, but rather due to differences in how the fitness function maps onto the actual distribution of phenotypes in a given population. We discuss these results in the light of previous work on reverse evolution, and the role of ancestry, chance, and past and ongoing selection in adaptive evolution.     

Sexual antagonism for testosterone maintains multiple mating behaviour

1. The persistence of multiple mating remains one of the fundamental questions in evolutionary biology. In theory, multiple mating is predicted to improve female fitness cumulatively through direct and/or genetic benefits. However, intra-locus sexual conflicts may potentially constrain or even eliminate these benefits owing to the gender load imposed by sexually antagonistic selection. 2. Here, we tested whether sexually antagonistic selection can maintain the variance in multiple mating behaviour of bank voles (Myodes glareolus) by manipulating the hormone testosterone through artificial selection in the laboratory. Among mammals, testosterone is a sexually dimorphic fitness-related trait under selection and is known to affect mating behaviour. We conducted mating trials in which females derived from family-based selection of testosterone were sequentially paired with four males of different testosterone profiles. 3. We show that artificial selection for high testosterone increased the mating rate of males, but clearly decreased the number of partners that females mated with (and vice versa). Because multiple mating was beneficial for the reproductive success of both sexes, as evidenced by the positive Bateman gradients, the divergent evolutionary interests of testosterone between the sexes can maintain this polygynandrous mating system. 4. Our results highlight how mating rate is concordantly selected in both sexes; however, it is largely influenced by testosterone, which is under sexually antagonistic selection. 5. This study is the first one to emphasise the direct and indirect effects of the endocrine system not only on reproductive physiology and behaviour but also for the evolution of genetic mating strategies in mammals.     

The maintenance of heritable variation through social competition

The paradoxical persistence of heritable variation for fitness-related traits is an evolutionary conundrum that remains a preeminent problem in evolutionary biology. Here we describe a simple mechanism in which social competition results in the evolutionary maintenance of heritable variation for fitness related traits. We demonstrate this mechanism using a genetic model with two primary assumptions: the expression of a trait depends upon success in social competition for limited resources; and competitive success of a genotype depends on the genotypes that it competes against. We find that such social competition generates heritable (additive) genetic variation for "competition-dependent" traits. This heritable variation is not eroded by continuous directional selection because, rather than leading to fixation of favored alleles, selection leads instead to allele frequency cycling due to the concerted coevolution of the social environment with the effects of alleles. Our results provide a mechanism for the maintenance of heritable variation in natural populations and suggest an area for research into the importance of competition in the genetic architecture of fitness related traits.     

STABILIZING SELECTION DETECTED FOR BRISTLE NUMBER IN DROSOPHILA MELANOGASTER

Stabilizing selection, which favors intermediate phenotypes, is frequently invoked as the selective force maintaining a population's status quo. Two main alternative reasons for stabilizing selection on a quantitative trait are possible: (1) intermediate trait values can be favored through the causal effect of the trait on fitness (direct stabilizing selection); or (2) through a pleiotropic, deleterious side effect on fitness of mutants affecting the trait (apparent stabilizing selection). Up to now, these alternatives have never been experimentally disentangled. Here we measure fitness as a function of the number of abdominal bristles within four Drosophila melanogaster lines, one with high, one with low, and two with intermediate average bristle number. The four were inbred nonsegregating lines, so that apparent selection due to pleiotropy is not possible. Individual fitness significantly increased (decreased) with bristles number in the low (high) line. No significant fitness-trait association was detected within each intermediate line. These results reveal substantial direct stabilizing selection on the trait.     

BEYOND REINFORCEMENT: THE EVOLUTION OF PREMATING ISOLATION BY DIRECT SELECTION ON PREFERENCES AND POSTMATING, PREZYGOTIC INCOMPATIBILITIES

Abstract The evolution of premating isolation after secondary contact is primarily considered in the guise of reinforcement, which relies on low hybrid fitness as the driving force for mating preference divergence. Here I consider two additional forces that may play a substantial role in the adaptive evolution of premating isolation, direct selection on preferences and indirect selection against postmating, prezygotic incompatibilities. First, I argue that a combination of ecological character displacement and sensory bias can cause direct selection on preferences that results in the pattern of reproductive character displacement. Both analytical and numerical methods are then used to demonstrate that, as expected from work in single populations, such direct selection will easily overwhelm indirect selection due to low hybrid fitness as the primary determinant of preference evolution. Second, postmating, prezygotic incompatibilities are presented as a driving force in the evolution of premating isolation. Two classes of these mechanisms, those increasing female mortality after mating but before producing offspring and those reducing female fertility, are shown to be identical in their effects on preference divergence. Analytical and numerical techniques are then used to demonstrate that postmating, prezygotic factors may place strong selection on preference divergence. These selective forces are shown to be comparable if not greater than those produced by the low fitness of hybrids.     

Fitness and evolution in clonal plants: the impact of clonal growth

Seeds have often been emphasized in estimates of plant fitness because they are the units that carry genes to the next generation, disperse, and found new populations. We contend that clonal growth also needs to be considered when estimating fitness in clonal plants, regardless of whether fitness is measured from a genet or ramet perspective. Clonal growth affects genet fitness through both genet persistence and seed production. It affects ramet fitness through new ramet production, because both seeds and clonal propagants are considered offspring. The differential production of clonal propagants will contribute to fitness differences among individuals which may result in population-level changes in allele frequencies (i.e. microevolution). We describe a form of selection unique to clonal organisms, genotypic selection, that can result in evolution. Genotypic selection occurs when genotypically based traits are associated with differences in the rate of ramet production. It can lead to evolutionary change in quantitative trait means both directly and indirectly. It leads directly to change in the ramet population by increasing the proportion of ramets with more advantageous trait values. From the genet perspective, it leads indirectly to evolution within and among populations whenever significant portions of the genetic effect on a trait are inherited through seed. We argue that under most conditions, clonal growth will play a major role in the microevolution of clonal plants.     

Inbreeding depression and genetic load of sexually selected traits: how the guppy lost its spots

To date, few studies have investigated the effects of inbreeding on sexually selected traits, although inbreeding depression on such traits can play an important role in the evolution and ecology of wild populations. Sexually selected traits such as ornamentation and courtship behaviour may not be primary fitness characters, but selection and dominance coefficients of their mutations will resemble those of traits under natural selection. Strong directional selection, for instance, through female mate-choice, purges all but the most recessive deleterious mutations, and the remaining dominance variation will result in inbreeding depression once populations undergo bottlenecks. We analysed the effects of inbreeding on sexually selected traits (colour pattern and courtship behaviour) in the male guppy, Poecilia reticulata, from Trinidad, and found a significant decline in the frequency of mating behaviour and colour spots. Such effects occurred although the genetic basis of these traits, many of which are Y-linked and hemizygous, would be expected to leave relatively little scope for inbreeding depression. Findings suggest that these sexually selected traits could reflect the genetic condition or health of males, and thus may be informative mate-cue characters for female choice as suggested by the 'good genes' model.