Phenotypic variation with respect to fitness: the basis for rank-order selection*

Having argued that phenotypic variation with respect to the component of fitness involved in withstanding density stress is useful for the persistence of populations through time, the sources of such variation are described. Age differences and differences caused by the accidental encounters of dissimilar microenvironments are non-genetic in origin. Genetic bases for phenotypic variation can either be proximate (each individual having a unique genotype) or ultimate. The latter case is one in which the genotypes of individuals are such that the progeny they produce are phenotypically variable. Selection favouring such genotypes can be shown to be Darwinian; group selection is not required. A means for revealing instances of the ultimate genetic control of phenotypic variation is suggested: measures of what should be error variance prove to be larger than those which should, under normal circumstances, include error variance. The last increment of variation that causes what might otherwise be repetitive structures to differ can be ascribed to decisions that are genetically pre-set within developmental programmes.     

The evolutionary significance of parasitism: do parasite‐driven genetic dynamics occur ex silico?

It has long been recognized that reciprocal antagonism might lock host and parasite populations into a process of constant change, adapting and reacting in open‐ended coevolution. A significant body of theory supports this intuition: dynamic genetic polymorphisms are a common outcome of computer simulations of host–parasite coevolution. These in silico experiments have also shown that dynamical interactions could be responsible for high levels of genetic diversity in host populations, and even be the principle determinant of rates of genetic recombination and sexuality. The evolutionary significance of parasitism depends on the strength and prevalence of parasite‐mediated selection in nature. Here I appraise whether parasitism is a pervasive agent of evolutionary change by detailing empirical evidence for selection. Although there is considerable evidence of genetic variation for resistance, and hence the potential for selection, direct observation of parasite‐driven genetic change is lacking.     

Local adaptation and cogradient selection in the alpine plant, Poa hiemata, along a narrow altitudinal gradient

Alpine environments are particularly susceptible to environmental changes associated with global warming but there is potential for alpine plants to adapt to warming if local adaptation occurs and gene flow allows genotypes adapted to low altitudes to colonize higher altitude sites. Here we examine the adaptive potential of a common alpine grass, Poa hiemata, within the restricted alpine habitat of Australian mountains, across a narrow altitudinal gradient replicated in three areas. Grasses at high altitude sites had shorter leaf lengths and larger circumferences than those at lower sites. Transplant experiments with clonal material and plants grown from seed indicated that these differences were partly genetic, with environmental and genetic factors both contributing to the differences between altitudes. Differences in altitudinal forms were also evident in a common garden experiment. Plants showed a home-site advantage in terms of survival. A fitness analysis indicated that at high altitude sites, selection favored plants with short leaves and larger circumferences, whereas these traits were selected in the opposite direction at the low altitude sites. These findings indicate cogradient selection and potential for both plastic and genotypic shifts in response to climate change in P. hiemata.     

Trade‐offs and evolution of thermal adaptation in the Irish potato famine pathogen Phytophthora infestans

Temperature is one of the most important environmental parameters with crucial impacts on nearly all biological processes. Due to anthropogenic activity, average air temperatures are expected to increase by a few degrees in coming decades, accompanied by an increased occurrence of extreme temperature events. Such global trends are likely to have various major impacts on human society through their influence on natural ecosystems, food production and biotic interactions, including diseases. In this study, we used a combination of statistical genetics, experimental evolution and common garden experiments to investigate the evolutionary potential for thermal adaptation in the potato late blight pathogen, Phytophthora infestans, and infer its likely response to changing temperatures. We found a trade‐off associated with thermal adaptation to heterogeneous environments in P. infestans, with the degree of the trade‐off peaking approximately at the pathogen's optimum growth temperature. A genetic trade‐off in thermal adaptation was also evidenced by the negative association between a strain's growth rate and its thermal range for growth, and warm climates selecting for a low pathogen growth rate. We also found a mirror effect of phenotypic plasticity and genetic adaptation on growth rate. At below the optimum, phenotypic plasticity enhances pathogen's growth rate but nature selects for slower growing genotypes when temperature increases. At above the optimum, phenotypic plasticity reduces pathogen's growth rate but natural selection favours for faster growing genotypes when temperature increases further. We conclude from these findings that the growth rate of P. infestans will only be marginally affected by global warming.     

Modifying effects of phenotypic plasticity on interactions among natural selection, adaptation and gene flow

Divergent natural selection, adaptive divergence and gene flow may interact in a number of ways. Recent studies have focused on the balance between selection and gene flow in natural populations, and empirical work has shown that gene flow can constrain adaptive divergence, and that divergent selection can constrain gene flow. A caveat is that phenotypic diversification may be under the direct influence of environmental factors (i.e. it may be due to phenotypic plasticity), in addition to partial genetic influence. In this case, phenotypic divergence may occur between populations despite high gene flow that imposes a constraint on genetic divergence. Plasticity may dampen the effects of natural selection by allowing individuals to rapidly adapt phenotypically to new conditions, thus slowing adaptive genetic divergence. On the other hand, plasticity may promote future adaptive divergence by allowing populations to persist in novel environments. Plasticity may promote gene flow between selective regimes by allowing dispersers to adapt to alternate conditions, or high gene flow may result in the selection for increased plasticity. Here I expand frameworks for understanding relationships among selection, adaptation and gene flow to include the effects of phenotypic plasticity in natural populations, and highlight its importance in evolutionary diversification.     

Experimental studies of adaptation in Clarkia xantiana. I. Sources of trait variation across a subspecies border

Abstract Both genetic differentiation and phenotypic plasticity might be expected to affect the location of geographic range limits. Co‐gradient variation (CoGV), plasticity that is congruent with genetic differentiation, may enhance performance at range margins, whereas its opposite, counter‐gradient variation (CnGV) may hinder performance. Here we report findings of reciprocal transplant experiments intended to tease apart the roles of differentiation and plasticity in producing phenotypic variation across a geographic border between two plant subspecies. Clarkia xantiana ssp. xantiana and C. xantiana ssp. parviflora are California‐endemic annuals that replace each other along a west‐east gradient of declining precipitation. We analyzed variation in floral traits, phenological traits, and vegetative morphological and developmental traits by sowing seeds of 18 populations (six of ssp. xantiana and 12 of ssp. parviflora) at three sites (one in each subspecies' exclusive range and one in the subspecies' contact zone), in two growing seasons (an exceptionally wet El Niño winter and a much drier La Niña winter). Significant genetic differences between subspecies appeared in 11 of 12 traits, and differences were of the same sign as in nature. These findings are consistent with the hypothesis that selection is responsible for subspecies differences. Geographic variation within subspecies over part of the spatial gradient mirrored between‐subspecies differences present at a larger scale. All traits showed significant plasticity in response to spatial and temporal environmental variation. Plasticity patterns ranged from spatial and temporal CoGV (e.g., in node of first flower), to spatial CnGV (e.g., in flowering time), to patterns that were neither CoGV nor CnGV (the majority of traits). Instances of CoGV may reflect adaptive plasticity and may serve to increase performance under year‐to‐year environmental variation and at sites near the subspecies border. However, the presence of spatial CnGV in some critical traits suggests that subspecies ranges may also be constrained by patterns of plasticity.     

Local adaptation with high gene flow: temperature parameters drive adaptation to altitude in the common frog (Rana temporaria)

Both environmental and genetic influences can result in phenotypic variation. Quantifying the relative contributions of local adaptation and phenotypic plasticity to phenotypes is key to understanding the effect of environmental variation on populations. Identifying the selective pressures that drive divergence is an important, but often lacking, next step. High gene flow between high‐ and low‐altitude common frog (Rana temporaria) breeding sites has previously been demonstrated in Scotland. The aim of this study was to assess whether local adaptation occurs in the face of high gene flow and to identify potential environmental selection pressures that drive adaptation. Phenotypic variation in larval traits was quantified in R. temporaria from paired high‐ and low‐altitude sites using three common temperature treatments. Local adaptation was assessed using Q_ST–F_ST analyses, and quantitative phenotypic divergence was related to environmental parameters using Mantel tests. Although evidence of local adaptation was found for all traits measured, only variation in larval period and growth rate was consistent with adaptation to altitude. Moreover, this was only evident in the three mountains with the highest high‐altitude sites. This variation was correlated with mean summer and winter temperatures, suggesting that temperature parameters are potentially strong selective pressures maintaining local adaptation, despite high gene flow.     

Rapid differentiation of plasticity in life history and morphology during invasive range expansion and concurrent local adaptation in the horned beetle Onthophagus taurus

Understanding the interplay between genetic differentiation, ancestral plasticity, and the evolution of plasticity during adaptation to environmental variation is critical to predict populations’ responses to environmental change. However, the role of plasticity in rapid adaptation in nature remains poorly understood. We here use the invasion of the horned beetle Onthophagus taurus in the United States during the last half century to study the contribution of ancestral plasticity and post-invasion evolution of plastic responses in rapid population differentiation. We document latitudinal variation in life history and morphology, including genetic compensation in development time and body size, likely adaptive responses to seasonal constraints in the North. However, clinal variation in development time and size was strongly dependent on rearing temperature, suggesting that population differentiation in plasticity played a critical role in successful adaptation on ecological timescales. Clinal variation in wing shape was independent of ancestral plasticity, but correlated with derived plasticity, consistent with evolutionary interdependence. In contrast, clinal variation in tibia shape aligned poorly with thermal plasticity. Overall, this study suggests that post-invasion evolution of plasticity contributed to range expansions and concurrent adaptation to novel climatic conditions.     

Antagonistic coevolution with parasites maintains host genetic diversity: an experimental test

Genetic variation in natural populations is a prime prerequisite allowing populations to respond to selection, but is under constant threat from forces that tend to reduce it, such as genetic drift and many types of selection. Haldane emphasized the potential importance of parasites as a driving force of genetic diversity. His theory has been taken for granted ever since, but despite numerous studies showing correlations between genetic diversity and parasitism, Haldane''s hypothesis has rarely been tested experimentally for unambiguous support. We experimentally staged antagonistic coevolution between the host Tribolium castaneum and its natural microsporidian parasite, Nosema whitei, to test for the relative importance of two separate evolutionary forces (drift and parasite-induced selection) on the maintenance of genetic variation. Our results demonstrate that coevolution with parasites indeed counteracts drift as coevolving populations had significantly higher levels of heterozygosity and allelic diversity. Genetic drift remained a strong force, strongly reducing genetic variation and increasing genetic differentiation in small populations. To our surprise, differentiation between the evolving populations was smaller when they coevolved with parasites, suggesting parallel balancing selection. Hence, our results experimentally vindicate Haldane''s original hypothesis 60 years after its conception.     

Bovine tuberculosis: the genetic basis of host susceptibility

The prevalence of bovine tuberculosis (BTB) in the UK remains a significant economic burden and problem for the agri-food industry. Much effort has been directed towards improving diagnostics, finding vaccine candidates and assessing the usefulness of badger culling. The contribution that host genotype makes to disease outcome has, until recently, been overlooked; yet, it is biologically untenable that genetic variation does not play a role. In this review, we highlight the evidence, past and present, for a role of host genetics in determining susceptibility to BTB in livestock. We then address some of the major issues surrounding the design of future studies tasked with finding the exact causative genetic variation underpinning the TB susceptibility phenotype. Finally, we discuss some of the potential future benefits, and problems, that a knowledge of the genetic component to BTB resistance/susceptibility may bring to the agricultural industries and the wider scientific community.     

Phenological mismatch drives selection on elevation,but not on slope,of breeding time plasticity in a wild songbird

Phenotypic plasticity is an important mechanism for populations to respond to fluctuating environments, yet may be insufficient to adapt to a directionally changing environment. To study whether plasticity can evolve under current climate change, we quantified selection and genetic variation in both the elevation (RN_E) and slope (RN_S) of the breeding time reaction norm in a long‐term (1973–2016) study population of great tits (Parus major). The optimal RN_E (the caterpillar biomass peak date regressed against the temperature used as cue by great tits) changed over time, whereas the optimal RN_S did not. Concordantly, we found strong directional selection on RN_E, but not RN_S, of egg‐laying date in the second third of the study period; this selection subsequently waned, potentially due to increased between‐year variability in optimal laying dates. We found individual and additive genetic variation in RN_E but, contrary to previous studies on our population, not in RN_S. The predicted and observed evolutionary change in RN_E was, however, marginal, due to low heritability and the sex limitation of laying date. We conclude that adaptation to climate change can only occur via micro‐evolution of RN_E, but this will necessarily be slow and potentially hampered by increased variability in phenotypic optima.     

Patterns of phenotypic and genetic variation for the plasticity of diapause incidence

Phenotypic plasticity describes an organism's ability to produce multiple phenotypes in direct response to its environmental conditions. Over the past 15 years empiricists have found that this plasticity frequently exhibits geographic variation and often possesses a significant heritable genetic basis. However, few studies have examined both of these aspects of plasticity simultaneously. Here, we examined both the geographic and genetic variations of the plasticity for diapause incidence (the proportion of eggs that enter an arrested state of development capable of surviving over the winter) relative to temperatures and photoperiods associated with long and short season environments across six populations of the striped ground cricket, Allonemobius socius, using a half-sibling split brood quantitative genetic design. We found that plasticity, as measured by the slope of the reaction norm, was greater in the southern-low altitude region (where populations are bivoltine) relative to the southern-high and northern-low altitude regions (where populations are univoltine). However, the heritability of plasticity was only significantly different from zero in univoltine populations that experienced "intermediate" natal season lengths. These patterns suggest that selection may favor the plasticity of diapause incidence in bivoltine regions, but act against plasticity in regions in which populations are univoltine. Furthermore, our data suggest that under "intermediate" natal season length conditions, the interplay between local adaptation and gene flow may keep the plasticity of diapause incidence low (but still significant) while maintaining its genetic variation. As such, this study not only provides a novel observation into the geographic variation of phenotypic plasticity, but also provides much needed groundwork for tests of its adaptive significance.     

Evolution in stressful environments II: adaptive value and costs of plasticity in response to low light in Sinapis arvensis

Plants possess a remarkable capacity to alter their phenotype in response to the highly heterogeneous light conditions they commonly encounter in natural environments. In the present study with the weedy annual plant Sinapis arvensis, we (a) tested for the adaptive value of phenotypic plasticity in morphological and life history traits in response to low light and (b) explored possible fitness costs of plasticity. Replicates of 31 half-sib families were grown individually in the greenhouse under full light and under low light (40% of ambient) imposed by neutral shade cloth. Low light resulted in a large increase in hypocotyl length and specific leaf area (SLA), a reduction in juvenile biomass and a delayed onset of flowering. Phenotypic selection analysis within each light environment revealed that selection favoured large SLA under low light, but not under high light, suggesting that the observed increase in SLA was adaptive. In contrast, plasticity in the other traits measured was maladaptive (i.e. in the opposite direction to that favoured by selection in the low light environment). We detected significant additive genetic variance in plasticity in most phenotypic traits and in fitness (number of seeds). Using genotypic selection gradient analysis, we found that families with high plasticity in SLA had a lower fitness than families with low plasticity, when the effect of SLA on fitness was statistically kept constant. This indicates that plasticity in SLA incurred a direct fitness cost. However, a cost of plasticity was only expressed under low light, but not under high light. Thus, models on the evolution of phenotypic plasticity will need to incorporate plasticity costs that vary in magnitude depending on environmental conditions.     

Evolutionary potential of Chamaecrista fasciculata in relation to climate change. I. Clinal patterns of selection along an environmental gradient in the great plains

Climate change will alter natural selection on native plant populations. Little information is available to predict how selection will change in the future and how populations will respond. Insight can be obtained by comparing selection regimes in current environments to selection regimes in environments similar to those predicted for the future. To mimic predicted temporal change in climate, three natural populations of the annual legume Chamaecrista fasciculata were sampled from a climate gradient in the Great Plains and progeny of formal crosses were reciprocally planted back into common gardens across this climate gradient. In each garden, native populations produced significantly more seed than the other populations, providing strong evidence of local adaptation. Phenotypic selection analysis conducted by site showed that plants with slower reproductive development, more leaves, and thicker leaves were favored in the most southern garden. Evidence of clinal variation in selection regimes was also found; selection coefficients were ordered according to the latitude of the common gardens. The adaptive value of native traits was indicated by selection toward the mean of local populations. Repeated clinal patterns in linear and nonlinear selection coefficients among populations and within and between sites were found. To the extent that temporal change in climate into the future will parallel the differences in selection across this spatial gradient, this study suggests that selection regimes will be displaced northward and different trait values will be favored in natural populations.     

The evolution of social interactions changes predictions about interacting phenotypes

In many traits involved in social interactions, such as courtship and aggression, the phenotype is an outcome of interactions between individuals. Such traits whose expression in an individual is partly determined by the phenotype of its social partner are called "interacting phenotypes." Quantitative genetic models suggested that interacting phenotypes can evolve much faster than nonsocial traits. Current models, however, consider the interaction between phenotypes of social partners as a fixed phenotypic response rule, represented by an interaction coefficient (ψ). Here, we extend existing theoretical models and incorporate the interaction coefficient as a trait that can evolve. We find that the evolution of the interaction coefficient can change qualitatively the predictions about the rate and direction of evolution of interacting phenotypes. We argue that it is crucial to determine whether and how the phenotypic response of an individual to its social partner can evolve to make accurate predictions about the evolution of traits involved in social interactions.     

A heuristic model on the role of plasticity in adaptive evolution: plasticity increases adaptation,population viability and genetic variation

An ongoing new synthesis in evolutionary theory is expanding our view of the sources of heritable variation beyond point mutations of fixed phenotypic effects to include environmentally sensitive changes in gene regulation. This expansion of the paradigm is necessary given ample evidence for a heritable ability to alter gene expression in response to environmental cues. In consequence, single genotypes are often capable of adaptively expressing different phenotypes in different environments, i.e. are adaptively plastic. We present an individual-based heuristic model to compare the adaptive dynamics of populations composed of plastic or non-plastic genotypes under a wide range of scenarios where we modify environmental variation, mutation rate and costs of plasticity. The model shows that adaptive plasticity contributes to the maintenance of genetic variation within populations, reduces bottlenecks when facing rapid environmental changes and confers an overall faster rate of adaptation. In fluctuating environments, plasticity is favoured by selection and maintained in the population. However, if the environment stabilizes and costs of plasticity are high, plasticity is reduced by selection, leading to genetic assimilation, which could result in species diversification. More broadly, our model shows that adaptive plasticity is a common consequence of selection under environmental heterogeneity, and hence a potentially common phenomenon in nature. Thus, taking adaptive plasticity into account substantially extends our view of adaptive evolution.     

烟粉虱对菜豆金黄花叶病毒属病毒的传播：病毒对媒介昆虫的适应

双生病毒科(Geminiviridae)菜豆金黄花叶病毒属病毒是一类重要的植物病毒,主要危害番茄、烟草、棉花等多种经济作物,自然条件下主要由介体昆虫烟粉虱Bemisia tabaci传播。菜豆金黄花叶病毒属病毒在田间的暴发受多种因素的影响,其中一个最重要的因素就是其介体昆虫烟粉虱。因此,明确烟粉虱在田间传播和扩散特定病毒中的作用及影响因素,对于解析病毒病流行的生物学基础具有重要意义。本文综述了烟粉虱对菜豆金黄花叶病毒属病毒的传播及影响因素,并讨论了病毒对媒介昆虫的适应及其机制。菜豆金黄花叶病毒属病毒和烟粉虱都为全球分布的有害生物,通过生物信息学的分析发现,两者都呈现地域相关的遗传多样性。而在生物学的研究中发现,烟粉虱隐存种往往对与其起源于同一地区的病毒具有较高的传播效率。这些发现为进一步解析烟粉虱对菜豆金黄花叶病毒属病毒的传播提供了重要的参考。     

Phenotypic variation and associated predation risk of juvenile common carp Cyprinus carpio

Juvenile common carp Cyprinus carpio were collected from 10 lakes with variable predator abundance over 4 months to evaluate if morphological defences increased with increasing predation risk. Cyprinus carpio dorsal and pectoral spines were longer and body depth was deeper when predators were more abundant, with differences becoming more pronounced from July to October. To determine if morphological plasticity successfully reduced predation risk, prey selection of largemouth bass Micropterus salmoides foraging on deep- and shallow-bodied C. carpio was evaluated in open and vegetated environments. Predators typically selected deep- over shallow-bodied phenotypes in open habitats and neutrally selected both phenotypes in vegetated habitats. When exposed to predators, shallow-bodied C. carpio phenotypes shoaled in open habitat, whereas deep-bodied phenotypes occupied vegetation. Although deep-bodied phenotypes required additional handling time, shallow-bodied phenotypes were more difficult to capture. These results suggest that juvenile C. carpio gradually develop deeper bodies and larger spines as predation risk increases. Morphological defences made it more difficult for predators to consume these prey but resulted in higher vulnerability to predation in some instances.     

The evolution of animal genitalia: distinguishing between hypotheses by single species studies

Rapid evolution of genitalia is one of the most general patterns of morphological diversification in animals. Despite its generality, the causes of this evolutionary trend remain obscure. Several alternative hypotheses have been suggested to account for the evolution of genitalia (notably the lock-and-key, pleiotropism, and sexual selection hypotheses). Here, I argue that thorough intraspecific studies are the key to gaining insight into the patterns and processes of genitalic evolution. Critical assumptions and predictions that may be used to distinguish between the different hypotheses are identified and discussed. However, current knowledge of selection on genitalia, or even of the degree of phenotypic and genotypic variability of genital morphology, is highly limited, allowing only a very tentative assessment of the various hypotheses. In-depth single species studies of current patterns and processes of selection on genitalia are badly needed, and a single species research program is briefly outlined.