VARIATION IN THE STRENGTH AND SOFTNESS OF SELECTION ON DELETERIOUS MUTATIONS

Deleterious alleles constantly enter populations through mutation. Understanding the nature of selection against such alleles is required to assess their impact on populations. In a subdivided population, two distinct aspects of selection are important: the strength and softness of selection. Using Drosophila melanogaster, we estimated both aspects of selection for each of eight loci across two environments. These data allow us to test conflicting predictions about the factors affecting the softness of selection. First, we show that the softness of selection is not determined by ecological conditions alone. Second, we find that resource limitation makes selection stronger but does not make it softer. Third, we find that wild‐type individuals tend to benefit more than mutants from being reared with competitors of low genetic quality. This means that selection is effectively “harder” on mutants than wild types. A model is presented showing that the sensitivities of mutants and wild types to local competitors differentially affect equilibrium mutation frequency and measures of load.     

Survival of the steepest: hypersensitivity to mutations as an adaptation to soft selection

Darwinian evolution favours genotypes with high fitness (‘survival of the fittest’). Models of quasi‐species evolution, however, suggest that in some cases selection may favour genotypes that are more robust against the impact of mutations (‘survival of the flattest’) even if these genotypes have lower fitness. I show that the opposite effect will be observed if competition occurs during development (e.g. among embryos or ovules) or before the adult phase (e.g. among the progeny of an individual). If viability is not affected by selection at these initial stages (soft selection), the genotypes that are more sensitive to the effects of mutations may increase in frequency because they get rid more easily of deleterious mutations. In a simple theoretical model of mutation and selection, genotypes located in steeper regions of the fitness surface are favoured (‘survival of the steepest’) even if they do not have higher viability, and even if they have slightly deleterious effects. Hypersensitive genes are potentially harmful for the individual, but with soft selection during the juvenile phase they persist in the genome because they reduce competition with their mutants. Soft selection occurs in practically all vascular plants and in many animals, therefore antirobustness may be a very common feature of the genome of multicellular organisms.     

Interplay between age‐based competitive asymmetries within the brood and direct competition between inbred and outbred offspring in a burying beetle

Theory suggests that intraspecific competition associated with direct competition between inbred and outbred individuals should be an important determinant of the severity of inbreeding depression. The reason is that, if outbred individuals are stronger competitors than inbred ones, direct competition should have a disproportionate effect on the fitness of inbred individuals. However, an individual's competitive ability is not only determined by its inbreeding status but also by competitive asymmetries that are independent of an individual's inbreeding status. When this is the case, such competitive asymmetries may shape the outcome of direct competition between inbred and outbred individuals. Here, we investigate the interface between age‐based competitive asymmetries within broods and direct competition between inbred and outbred offspring in the burying beetle Nicrophorus vespilloides. We found that inbred offspring had lower survival than outbred ones confirming that there was inbreeding depression. Furthermore, seniors (older larvae) grew to a larger size and had higher survival than juniors (younger larvae), confirming that there were age‐based competitive asymmetries. Nevertheless, there was no evidence that direct competition between inbred and outbred larvae exacerbated inbreeding depression, no evidence that inbreeding depression was more severe in juniors and no evidence that inbred juniors suffered disproportionately due to competition from outbred seniors. Our results suggest that direct competition between inbred and outbred individuals does not necessarily exacerbate inbreeding depression and that inbred individuals are not always more sensitive to poor and stressful conditions than outbred ones.     

Genotype‐by‐environment interactions due to antibiotic resistance and adaptation in Escherichia coli

Mutations that are beneficial in one environment can have different fitness effects in other environments. In the context of antibiotic resistance, the resulting genotype‐by‐environment interactions potentially make selection on resistance unpredictable in heterogeneous environments. Furthermore, resistant bacteria frequently fix additional mutations during evolution in the absence of antibiotics. How do these two types of mutations interact to determine the bacterial phenotype across different environments? To address this, I used Escherichia coli as a model system, measuring the effects of nine different rifampicin resistance mutations on bacterial growth in 31 antibiotic‐free environments. I did this both before and after approximately 200 generations of experimental evolution in antibiotic‐free conditions (LB medium), and did the same for the antibiotic‐sensitive wild type after adaptation to the same environment. The following results were observed: (i) bacteria with and without costly resistance mutations adapted to experimental conditions and reached similar levels of competitive fitness; (ii) rifampicin resistance mutations and adaptation to LB both indirectly altered growth in other environments; and (iii) resistant‐evolved genotypes were more phenotypically different from the ancestor and from each other than resistant‐nonevolved and sensitive‐evolved genotypes. This suggests genotype‐by‐environment interactions generated by antibiotic resistance mutations, observed previously in short‐term experiments, are more pronounced after adaptation to other types of environmental variation, making it difficult to predict long‐term selection on resistance mutations from fitness effects in a single environment.     

Experimental evolution of protozoan traits in response to interspecific competition

Decades of experiments have demonstrated the ecological effect of competition, but experimental evidence for competitive effects on trait evolution is rare. I measured the evolution of six protozoan traits in response to competitors from the inquiline community of pitcher plants. Replicate populations of Colpoda, a ciliated protozoan, were allowed to evolve in response to intra- and interspecific competition for 20 days (approximately 100 generations), before traits were measured in two common garden environments. Populations that evolved with interspecific competition had smaller cell sizes, produced fewer cysts and had higher population growth rates relative to populations grown in monoculture. The presence of interspecific competitors led to differential lineage sorting, most likely by increasing the strength of selection. These results are the first to demonstrate protozoan evolution in response to competition and may have implications for species coexistence in this system.     

Ecological release exposes genetically based niche variation

The evolutionary trajectories of ecological niches have profound impacts on community, population and speciation dynamics, yet the underlying causes of niche lability vs. stasis are poorly understood. Here, we conducted a field experiment to quantify the effects of competition and, conversely, competitive release on the microevolutionary processes driving microhabitat niche evolution in an annual plant population restricted to California vernal pool wetlands. Removing competitors generated a strong increase in mean fitness, the exposure of genetically based niche variation and directional selection for niche evolution in the experimental population. In contrast, genetic variation in the microhabitat niche and directional selection for niche evolution were not detected in individuals growing with competitors. These results indicate that ecological opportunity (here, the removal of competitors) can trigger the immediate expression of latent, heritable niche variation that is necessary for rapid evolutionary responses; conversely, competitors may restrict niche evolution, contributing to niche conservatism in saturated communities.     

Reduced competitive ability in an invasive plant

One explanation for successful plant invaders is that they evolved to be more competitive. An intuitive prediction of this Evolution of Increased Competitive Ability (EICA) hypothesis never previously tested is that invasive populations should outcompete their native ‘ancestors’ in a common environment. We tested this idea in a diallel competition experiment with Alliaria petiolata where offspring from native and invasive populations were grown alone or in all pairwise combinations. While without competition, there were no differences between native and invasive populations, native populations outperformed invasive ones when competing against each other. Our results contradict the EICA hypothesis and we conclude that it does not not hold for Alliaria petiolata. Instead, we formulate a new ERCA (Evolutionary Reduced Competitive Ability) hypothesis: if there is less competition in the invasive range and competitive ability involves traits that have a fitness cost, then selection might act against it, thereby reducing intraspecific interactions too.     

An experimental test of character displacement's role in promoting postmating isolation between conspecific populations in contrasting competitive environments

Ecological character displacement takes place when two closely related species co-occur in only part of their geographical range, and selection to minimize competition between them promotes divergence in resource-use traits in sympatry but not in allopatry. Because populations sympatric with the heterospecific competitor will experience a different competitive environment than conspecific populations in allopatry, conspecific populations from these two competitive environments will also diverge in resource traits as an indirect consequence of interspecific ecological character displacement. Ultimately, ecologically dependent postmating isolation may arise between conspecific populations from these divergent competitive environments if offspring produced by matings between them are competitively inferior in either type of competitive environment. Yet, there are no direct tests of character displacement's role in initiating such postmating isolation. Here, we present a test by comparing the phenotypes and performances of spadefoot toad tadpoles produced from between-competitive-environment (BCE) matings versus those produced from within-competitive-environment (WCE) matings. When raised with naturally occurring competitors, BCE offspring grew significantly less and were significantly smaller than WCE offspring. BCE offspring generally performed worse even when raised alone, suggesting that they may have harbored intrinsic genetic incompatibilities. Moreover, the difference in growth and body size of BCE versus WCE offspring was significantly greater when each was raised with competitors than when each was raised alone, suggesting that BCE tadpoles were competitively inferior to WCE tadpoles. Presumably, this enhanced difference arose because BCE tadpoles produced an intermediate resource-use phenotype that is less well adapted to either competitive environment. Because larval size is under strong, positive, directional selection, reduced growth and size of BCE offspring may diminish gene flow between populations in divergent competitive environments, thereby generating postmating isolation. Thus, postmating isolation between conspecific populations, and possibly even speciation, may arise as a by-product of interactions between species.     

Sexual selection and assortative mating: an experimental test

Mate choice and mate competition can both influence the evolution of sexual isolation between populations. Assortative mating may arise if traits and preferences diverge in step, and, alternatively, mate competition may counteract mating preferences and decrease assortative mating. Here, we examine potential assortative mating between populations of Drosophila pseudoobscura that have experimentally evolved under either increased (‘polyandry’) or decreased (‘monogamy’) sexual selection intensity for 100 generations. These populations have evolved differences in numerous traits, including a male signal and female preference traits. We use a two males: one female design, allowing both mate choice and competition to influence mating outcomes, to test for assortative mating between our populations. Mating latency shows subtle effects of male and female interactions, with females from the monogamous populations appearing reluctant to mate with males from the polyandrous populations. However, males from the polyandrous populations have a significantly higher probability of mating regardless of the female's population. Our results suggest that if populations differ in the intensity of sexual selection, effects on mate competition may overcome mate choice.     

Characterizing selection in black‐throated blue warblers using a sexual network approach

Our understanding of trait evolution is built upon studies that examine the correlation between traits and fitness, most of which implicitly assume all individuals experience similar selective environments. However, accounting for differences in selective pressures, such as variation in the social environment, can advance our understanding of how selection shapes individual traits and subsequent fitness. In this study, we test whether variation in the social environment affects selection on individual phenotype. We apply a new sexual network framework to quantify each male's social environment as the mean body size of his primary competitors. We test for direct and social selection on male body size using a 10‐year data set on black‐throated blue warblers (Setophaga caerulescens), a territorial species for which body size is hypothesized to mediate competition for mates. We found that direct selection on body size was weak and nonsignificant, as was social selection via the body size of the males' competitors. Analysing both types of selection simultaneously allows us to firmly reject a role for body size in competitive interactions between males and subsequent male fitness in this population. We evaluate the application of the sexual network approach to empirical data and suggest that other phenotypic traits such as song characteristics and plumage may be more relevant than body size for male–male competition in this small passerine bird.     

Sex increases the probability of evolutionary rescue in the presence of a competitor

The explanation for the continued existence of sex, despite its many costs, remains one of the major challenges of evolutionary biology. Previous experimental studies have demonstrated that sex increases the rate of adaptation in novel environments relative to asexual reproduction. Whereas these studies have investigated the impact of sex on adaptation to stressful abiotic environments, the potential for biotic interactions to influence this advantage of sex has been largely ignored. Species rarely exist in isolation in natural conditions, so the impact of sex on adaptation to a stressful abiotic environment may be altered by the interactions between coexisting species. To investigate the interplay of sex and competition on adaptation to deteriorating conditions, we allowed populations of the unicellular alga (Chlamydomonas reinhardtii) to evolve in an environment to which they were initially poorly adapted. We manipulated both their mode of reproduction and the presence of a competitor, and monitored population size and proportion of evolutionary rescue events for each mode of reproduction. The results indicate that sex may be the beneficial strategy in the presence of the competitor. Sexual populations had highest probability of evolutionary rescue irrespective of the presence of the competitor. The overall advantage of sex was also manifested through higher level of adaptedness of survived sexual populations relative to asexual populations. Since competitive interactions are commonplace in nature, one of the explanations for the maintenance of sex by natural selection may be the increased rate of adaptation of sexual populations both in the presence and absence of competitors.     

How competition affects evolutionary rescue

Populations facing novel environments can persist by adapting. In nature, the ability to adapt and persist will depend on interactions between coexisting individuals. Here we use an adaptive dynamic model to assess how the potential for evolutionary rescue is affected by intra- and interspecific competition. Intraspecific competition (negative density-dependence) lowers abundance, which decreases the supply rate of beneficial mutations, hindering evolutionary rescue. On the other hand, interspecific competition can aid evolutionary rescue when it speeds adaptation by increasing the strength of selection. Our results clarify this point and give an additional requirement: competition must increase selection pressure enough to overcome the negative effect of reduced abundance. We therefore expect evolutionary rescue to be most likely in communities which facilitate rapid niche displacement. Our model, which aligns to previous quantitative and population genetic models in the absence of competition, provides a first analysis of when competitors should help or hinder evolutionary rescue.     

Priority effects and habitat complexity affect the strength of competition

Both habitat complexity and priority effects can influence the strength of competitive interactions; however, the independent and synergistic effects of these processes are not well understood. In Moorea, French Polynesia, we conducted a factorial field experiment to quantify the independent and combined effects of priority effects and habitat complexity on the strength of intraspecific competitive interactions among recently settled individuals of a coral reef fish (Thalassoma quinquevittatum: Labridae). Simultaneous arrival of focal individuals with competitors resulted in a 2.89-fold increase in survival relative to reefs where focal individuals arrived 5 days later than competitors (i.e., a priority effect). Increasing habitat complexity resulted in a 1.55-fold increase in survivorship when focal individuals arrived simultaneously with or before competitors. However, increasing habitat complexity did not affect the survivorship of focal individuals arriving 5 days later than competitors. Behavior observations showed that survivorship was negatively correlated with aggression. Aggression by prior residents towards focal individuals was significantly greater when focal individuals arrived 5 days later than competitors than when they arrived simultaneously. Increasing habitat complexity did not reduce aggression. Our results suggest that, when competitors arrive simultaneously, competitive interactions are weak and subordinates are not displaced from complex habitat; increasing habitat complexity increases survival by disrupting predation. Conversely, when competitors arrive at different times, aggression intensifies and increasing habitat complexity does not disrupt predation because competitive subordinates are excluded from habitat resources. This study demonstrates that the strength of competition can be context-dependent and may vary with the timing of competitive interactions and habitat complexity.     

Alternative forms of competition and predation dramatically affect habitat selection under foraging--predation-risk trade-offs

Habitat selection under foraging—predation-risk trade-offshas been a frequent topic of interest to theoretical behavioraland evolutionary ecologists. However, most habitat selectionmodels assume that individuals compete exploitatively for resourcesand that predation is either density independent or dilutedcompletely by competitor number, despite empirical evidencethat other forms of competition and predation also occur innature. I developed an individual-based model for studyingthe effects of alternative forms of competition and predationon the process of habitat selection under foraging—predation-risktrade-offs. To make the model more relevant to natural populations,I assumed that individuals vary continuously in traits relatedto competitive ability and vulnerability to predation and allowed resources and predators to be distributed across more than twohabitats. The results of my investigation demonstrate thatthe predicted pattern of habitat selection can be affecteddramatically by the form predation is assumed to take. Whenpredation is density dependent or frequency dependent, individuals will tend to be distributed across habitats according to theirabsolute vulnerability to predation. In contrast, when predationis density dependent or vulnerability dependent, individualswill tend to segregate by competitive ability. Whether oneassumes that individuals compete for resources via exploitationor interference also influences the predicted pattern of habitat selection. In general, interference competition results in amore even distribution of competitors across habitats.     

Bacteriocins and the assembly of natural Pseudomonas fluorescens populations

When competing for space and resources, bacteria produce toxins known as bacteriocins to gain an advantage over competitors. Recent studies in the laboratory have confirmed theoretical predictions that bacteriocin production can determine coexistence, by eradicating sensitive competitors or driving the emergence of resistant genotypes. However, there is currently limited evidence that bacteriocin‐mediated competition influences the coexistence and distribution of genotypes in natural environments, and what factors drive interactions towards inhibition remain unclear. Using natural soil populations of Pseudomonas fluorescens, we assessed the ability of the isolates to inhibit one another with respect to spatial proximity in the field, genetic similarity and niche overlap. The majority of isolates were found to produce bacteriocins; however, widespread resistance between coexisting isolates meant relatively few interactions resulted in inhibition. When inhibition did occur, it occurred more frequently between ecologically similar isolates. However, in contrast with results from other natural populations, we found no relationship between the frequency of inhibition and the genetic similarity of competitors. Our results suggest that bacteriocin production plays an important role in mediating competition over resources in natural settings and, by selecting for isolates resistant to local bacteriocin production, can influence the assembly of natural populations of P. fluorescens.     

Interspecific competition in perennial sedentary organisms: An individual-based model

We investigated a mathematical model of the dynamics of the ecological system consisting of two competing perennial species, each of which leads a sedentary life. It is an individual-based model, in which the growth of each individual is described. The rate of this growth is weakened by competition from neighboring individuals. The strength of the competitors' influence depends on their size and distance to them. The conditions, in which the competitive exclusion of one of the competitors and the coexistence of both competitors take place are provided. The influence of the parameters responsible for the strength of competition, the degree of competitive asymmetry, and consideration of the importance of specific elements of the spatial structure of this ecological system on the results of the competition were analyzed. Both species co-exist when they are equal competitors. Permanent coexistence is possible only when interspecific competition is weaker than intraspecific. When interspecific competition is stronger, the coexistence of equal interspecific competitors is random. Both species have equal probability of extinction. If species are not equal competitors, the stronger one wins. This result can be modified by different strengths of intraspecific competition. The weaker interspecific competitor can permanently coexist with stronger one, when its individuals suffer stronger intraspecific competition.     

Two-species asymmetric competition: effects of age structure on intra- and interspecific interactions

1. The patterns of density-dependent resource competition and the mechanisms leading to competitive exclusion in an experimental two-species insect age-structured interaction were investigated. 2. The modes of competition (scramble or contest) and strength of competition (under- to overcompensatory) operating within and between the stages of the two species was found to be influenced by total competitor density, the age structure of the competitor community and whether competition is between stages of single or two species. 3. The effect of imposed resource limitation on survival was found to be asymmetric between stages and species. Environments supporting both dominant and subordinate competitors were found to increase survival of subordinate competitors at lower total competitor densities. Competitive environments during development within individual stage cohorts (i.e. small or large larvae), differed from the competitive environment in lumped age classes (i.e. development from egg-->pupae). 4. Competition within mixed-age, stage or species cohorts, when compared with uniform-aged or species cohorts, altered the position of a competitive environment on the scramble-contest spectrum. In some cases the competitive environment switched from undercompensatory contest to overcompensatory scramble competition. 5. Such switching modes of competition suggest that the relative importance of the mechanisms regulating single-species population dynamics (i.e. resource competition) may change when organisms are embedded within a wider community.     

Relative importance of competition and plant–soil feedback,their synergy,context dependency and implications for coexistence

Plants interact simultaneously with each other and with soil biota, yet the relative importance of competition vs. plant–soil feedback (PSF) on plant performance is poorly understood. Using a meta‐analysis of 38 published studies and 150 plant species, we show that effects of interspecific competition (either growing plants with a competitor or singly, or comparing inter‐ vs. intraspecific competition) and PSF (comparing home vs. away soil, live vs. sterile soil, or control vs. fungicide‐treated soil) depended on treatments but were predominantly negative, broadly comparable in magnitude, and additive or synergistic. Stronger competitors experienced more negative PSF than weaker competitors when controlling for density (inter‐ to intraspecific competition), suggesting that PSF could prevent competitive dominance and promote coexistence. When competition was measured against plants growing singly, the strength of competition overwhelmed PSF, indicating that the relative importance of PSF may depend not only on neighbour identity but also density. We evaluate how competition and PSFs might interact across resource gradients; PSF will likely strengthen competitive interactions in high resource environments and enhance facilitative interactions in low‐resource environments. Finally, we provide a framework for filling key knowledge gaps and advancing our understanding of how these biotic interactions influence community structure.     

The correlation between coloration and exploration behaviour varies across hierarchical levels in a wild passerine bird

In vertebrates, darker individuals are often found to be more active and willing to take risks (representing characteristics of a ‘proactive’ coping style), whereas lighter individuals are instead more cautious and less active (representing characteristics of a ‘reactive’ coping style). It is thus generally expected that melanin‐based coloration and proactivity form a suite of positively integrated traits at the among‐individual level. Here, we use a multigenerational pedigree of free‐living great tits (Parus major) to partition variation in, and the correlation between, melanin‐based breast stripe (‘tie’) size and exploration behaviour (a proxy for coping style) into its among‐ and within‐individual components. We show that both traits harbour heritable variation. Against predictions, tie size and speed of exploration were negatively correlated at the among‐individual level due to the combined influences of permanent environmental and additive genetic effects. By contrast, the two traits were weakly positively correlated within individuals (i.e. individuals increasing in tie size after moult tended to become more explorative). The patterns of among‐individual covariance were not caused by correlational selection as we found additive and opposite selection pressures acting on the two traits. These findings imply that testing hypotheses regarding the existence of a ‘syndrome’ at the among‐individual level strictly requires variance partitioning to avoid inappropriate interpretations as the negative ‘unpartitioned’ phenotypic correlation between exploration and tie size resulted from counteracting effects of within‐ and among‐individual correlations. Identifying sources and levels of (co)variation in phenotypic traits is thus critical to our understanding of biological patterns and evolutionary processes.     

Social competition as a driver of phenotype–environment correlations: implications for ecology and evolution

While it is universally recognised that environmental factors can cause phenotypic trait variation via phenotypic plasticity, the extent to which causal processes operate in the reverse direction has received less consideration. In fact individuals are often active agents in determining the environments, and hence the selective regimes, they experience. There are several important mechanisms by which this can occur, including habitat selection and niche construction, that are expected to result in phenotype–environment correlations (i.e. non-random assortment of phenotypes across heterogeneous environments). Here we highlight an additional mechanism – intraspecific competition for preferred environments – that may be widespread, and has implications for phenotypic evolution that are currently underappreciated. Under this mechanism, variation among individuals in traits determining their competitive ability leads to phenotype–environment correlation; more competitive phenotypes are able to acquire better patches. Based on a concise review of the empirical evidence we argue that competition-induced phenotype–environment correlations are likely to be common in natural populations before highlighting the major implications of this for studies of natural selection and microevolution. We focus particularly on two central issues. First, competition-induced phenotype–environment correlation leads to the expectation that positive feedback loops will amplify phenotypic and fitness variation among competing individuals. As a result of being able to acquire a better environment, winners gain more resources and even better phenotypes – at the expense of losers. The distinction between individual quality and environmental quality that is commonly made by researchers in evolutionary ecology thus becomes untenable. Second, if differences among individuals in competitive ability are underpinned by heritable traits, competition results in both genotype–environment correlations and an expectation of indirect genetic effects (IGEs) on resource-dependent life-history traits. Theory tells us that these IGEs will act as (partial) constraints, reducing the amount of genetic variance available to facilitate evolutionary adaptation. Failure to recognise this will lead to systematic overestimation of the adaptive potential of populations. To understand the importance of these issues for ecological and evolutionary processes in natural populations we therefore need to identify and quantify competition-induced phenotype–environment correlations in our study systems. We conclude that both fundamental and applied research will benefit from an improved understanding of when and how social competition causes non-random distribution of phenotypes, and genotypes, across heterogeneous environments.