Carry‐over effects of conditions at the wintering grounds on breeding plumage signals in a migratory bird: roles of phenotypic plasticity and selection

To understand the consequences of ever‐changing environment on the dynamics of phenotypic traits, distinguishing between selection processes and individual plasticity is crucial. We examined individual consistency/plasticity in several male secondary sexual traits expressed during the breeding season (white wing and forehead patch size, UV reflectance of white wing patch and dorsal melanin coloration) in a migratory pied flycatcher (Ficedula hypoleuca) population over an 11‐year period. Furthermore, we studied carry‐over effects of three environmental variables (NAO, a climatic index; NDVI, a vegetation index; and rainfall) at the wintering grounds (during prebreeding moult) on the expression of these breeding plumage traits of pied flycatcher males at individual and population levels. Whereas NAO correlates negatively with moisture in West Africa, NDVI correlates positively with primary production. Forehead patch size and melanin coloration were highly consistent within individuals among years, whereas the consistency of the other two traits was moderate. Wing patch size decreased with higher NAO and increased with higher rainfall and NDVI at the individual level. Interestingly, small‐patched males suffered lower survival during high NAO winters than large‐patched males, and vice versa during low NAO winters. These counteracting processes meant that the individual‐level change was masked at the population level where no relationship was found. Our results provide a good example of how variation in the phenotypic composition of a natural population can be a result of both environment‐dependent individual plasticity and short‐term microevolution. Moreover, when plasticity and viability selection operate simultaneously, their impacts on population composition may not be evident.     

Context-dependent sexual advertisement: plasticity in development of sexual ornamentation throughout the lifetime of a passerine bird

Male investment into sexual ornamentation is a reproductive decision that depends on the context of breeding and life history state. In turn, selection for state- and context-specific expression of sexual ornamentation should favour the evolution of developmental pathways that enable the flexible allocation of resources into sexual ornamentation. We studied lifelong variation in the expression and condition-dependence of a sexual ornament in relation to age and the context of breeding in male house finches (Carpodacus mexicanus)--a species that develops a new sexual ornament once a year after breeding. Throughout males' lifetime, the elaboration of ornamentation and the allocation of resources to the development of sexual ornamentation depended strongly on pairing status in the preceding breeding season--males that were single invested more resources into sexual ornamentation and changed ornamentation more than males that were paired. During the initial (post-juvenile) moult, the expression of ornamentation was closely dependent on individual condition, however the condition-dependence of ornamentation sharply decreased throughout a male's lifetime and in older males expression of sexual ornamentation was largely independent of condition during moult. Selection for early breeding favoured greater ornamentation in males that were single in the preceding seasons and the strength of this selection increased with age. On the contrary, the strength of selection on sexual ornamentation decreased with age in males that were paired in the preceding breeding season. Our results reveal strong context-dependency in investment into sexual ornamentation as well as a high flexibility in the development of sexual ornamentation throughout a male's life.     

The role of phenotypic plasticity in responses of hunted thinhorn sheep ram horn growth to changing climate conditions

When phenotypic change occurs over time in wildlife populations, it can be difficult to determine to what degree it is because of genetic effects or phenotypic plasticity. Here, we assess phenotypic changes over time in horn length and volume of thinhorn sheep (Ovis dalli) rams from Yukon Territory, Canada. We considered 42 years of horn growth from over 50 000 growth measurements in over 8000 individuals. We found that weather explained a large proportion of the annual fluctuation in horn growth, being particularly sensitive to spring weather. Only 2.5% of variance in horn length growth could be explained by an individual effect, and thus any genetic changes over the time period could only have had a small effect on phenotypes. Our findings allow insight into the capacity for horn morphology to react to selection pressures and demonstrate the overall importance of climate in determining growth.     

Phenotypic plasticity: Eco-Devo and evolution

Phenotypic plasticity refers to the ability of an organism to alter its physiology/morphology/behavior in response to changes in environmental conditions. Although encompassing various phenomena spanning multi-ple levels of organization, most plastic responses seem to take place by altering gene expression and eventually altering ontogenetic trajectory in response to environmental variation. Epigenetic modifications provide a plausi-ble link between the environment and alterations in gene expression, and the alterations in phenotype based on environmentally induced epigenetic modifications can be inherited transgenerationally. Even closely related species and populations with different genotypes may exhibit differences in the patterns and the extents of plastic responses, indicating the wide existence of plasticity genes which are independent of trait means and directly respond to environmental stimuli by triggering phenotypic changes. The ability of plasticity is not only able to affect the adaptive evolution of species significantly, but is also an outcome of evolutionary processes. Therefore, phenotypic plasticity is a potentially important molder of adaptation and evolution.     

Phenotypic plasticity facilitates initial colonization of a novel environment

Phenotypic plasticity can allow organisms to respond to environmental changes by producing better matching phenotypes without any genetic change. Because of this, plasticity is predicted to be a major mechanism by which a population can survive the initial stage of colonizing a novel environment. We tested this prediction by challenging wild Drosophila melanogaster with increasingly extreme larval environments and then examining expression of alcohol dehydrogenase (ADH) and its relationship to larval survival in the first generation of encountering a novel environment. We found that most families responded in the adaptive direction of increased ADH activity in higher alcohol environments and families with higher plasticity were also more likely to survive in the highest alcohol environment. Thus, plasticity of ADH activity was positively selected in the most extreme environment and was a key trait influencing fitness. Furthermore, there was significant heritability of ADH plasticity that can allow plasticity to evolve in subsequent generations after initial colonization. The adaptive value of plasticity, however, was only evident in the most extreme environment and had little impact on fitness in less extreme environments. The results provide one of the first direct tests of the adaptive role of phenotypic plasticity in colonizing a novel environment.     

Biological responses to environmental heterogeneity under future ocean conditions

Organisms are projected to face unprecedented rates of change in future ocean conditions due to anthropogenic climate‐change. At present, marine life encounters a wide range of environmental heterogeneity from natural fluctuations to mean climate change. Manipulation studies suggest that biota from more variable marine environments have more phenotypic plasticity to tolerate environmental heterogeneity. Here, we consider current strategies employed by a range of representative organisms across various habitats – from short‐lived phytoplankton to long‐lived corals – in response to environmental heterogeneity. We then discuss how, if and when organismal responses (acclimate/migrate/adapt) may be altered by shifts in the magnitude of the mean climate‐change signal relative to that for natural fluctuations projected for coming decades. The findings from both novel climate‐change modelling simulations and prior biological manipulation studies, in which natural fluctuations are superimposed on those of mean change, provide valuable insights into organismal responses to environmental heterogeneity. Manipulations reveal that different experimental outcomes are evident between climate‐change treatments which include natural fluctuations vs. those which do not. Modelling simulations project that the magnitude of climate variability, along with mean climate change, will increase in coming decades, and hence environmental heterogeneity will increase, illustrating the need for more realistic biological manipulation experiments that include natural fluctuations. However, simulations also strongly suggest that the timescales over which the mean climate‐change signature will become dominant, relative to natural fluctuations, will vary for individual properties, being most rapid for CO₂ (~10 years from present day) to 4 decades for nutrients. We conclude that the strategies used by biota to respond to shifts in environmental heterogeneity may be complex, as they will have to physiologically straddle wide‐ranging timescales in the alteration of ocean conditions, including the need to adapt to rapidly rising CO₂ and also acclimate to environmental heterogeneity in more slowly changing properties such as warming.     

Phenotypic plasticity and integration in response to flooded conditions in natural accessions of Arabidopsis thaliana (L.) Heynh (Brassicaceae)

Flood response is a crucial component of the life strategy of many plants, but it is seldom studied in non-flooded tolerant species, even though they may be subjected to stressful environmental conditions. Phenotypic plasticity in reaction to environmental stress affects the whole plant phenotype and can alter the character correlations that constitute the phenotypic architecture of the individual, yet few studies have investigated the lability of phenotypic integration to water regime. Moreover, little has been done to date to quantify the sort of selective pressures that different components of a plant's phenotype may be experiencing under contrasting water regimes. Genetic differentiation and phenotypic plasticity at the single-trait and multivariate levels were investigated in 47 accessions of the weedy plant Arabidopsis thaliana, and the relationship of plastic characters to reproductive fitness was quantified. Results indicate that these plants tend to be highly genetically differentiated for all traits, in agreement with predictions made on the basis of environmental variation and mating system. Varied patterns of apparent selection under flooded and non-flooded conditions were also uncovered, suggesting trade-offs in allocation between roots and above-ground biomass, as well as between leaves and reproductive structures. While the major components of the plants' multivariate phenotypic architecture were not significantly affected by environmental changes, many of the details were different under flooded and non-flooded conditions.     

Lifetime individual plasticity in body condition of a migratory bird

Body condition is an important trait that reflects the capacity of individuals to acquire food or resist disease, eventually allowing successful reproduction and survival. We first quantified the effects of condition on life history and a secondary sexual trait using long‐term lifetime data on condition in a migratory bird species, the barn swallow, Hirundo rustica. Second, we quantified sources of individual variation in condition by separating the within‐individual from the between‐individual components of variation of environmental condition and age on body condition. Therefore, we were able to partition variation as a result of selection and phenotypic plasticity. Within‐individual variation in body condition increased in early life until middle age (i.e. 3–4 years of age) in the two sexes followed by only a slight decrease in body condition during senescence in males but not in females. After accounting for age‐dependent variation, condition could be partitioned into a within‐individual plastic response to environmental conditions during migration and a nonplastic response (i.e. a between‐individual difference) to environmental conditions experienced in the African winter quarters. Specifically, there was a within‐individual increase in body condition as environmental conditions during migration improved in both males and females, independent of age. There was a between‐individual effect of condition found in the winter quarter in body condition of females, but not in males, which was attributed to the disappearance of females in poor body condition from the study population as a result of the higher natal dispersal of low‐quality females compared to high‐quality ones during years with favourable environmental conditions in the African winter quarters. Males and females also tended to be in better body condition during the warmer springs upon arrival at the breeding grounds. There was a temporal decline in female body condition during 1991–2007, whereas no significant trend was detected in males. Therefore, both intrinsic (e.g. age and sex) and extrinsic factors (e.g. climate) affected body condition. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105 , 420–434.     

Phenotypic plasticity as a state-dependent life-history decision

Summary A genotype is said to show phenotypic plasticity if it can produce a range of environmentally dependent phenotypes. Plasticity may or may not be adaptive. We consider plasticity as a genetically determined trait and thus find the optimal response of an animal to its environment. Various aspects of this optimal response are illustrated with examples based on reproductive effort. We investigate the selection pressure for plastic as opposed to fixed strategies. An example with spatial heterogeneity is used to compare our approach with that of Stearns and Koella (1986).     

Factors influencing plasticity in the arrival‐breeding interval in a migratory species reacting to climate change

Climate change is profoundly affecting the phenology of many species. In migratory birds, there is evidence for advances in their arrival time at the breeding ground and their timing of breeding, yet empirical studies examining the interdependence between arrival and breeding time are lacking. Hence, evidence is scarce regarding how breeding time may be adjusted via the arrival‐breeding interval to help local populations adapt to local conditions or climate change. We used long‐term data from an intensively monitored population of the northern wheatear (Oenanthe oenanthe) to examine the factors related to the length of 734 separate arrival‐to‐breeding events from 549 individual females. From 1993 to 2017, the mean arrival and egg‐laying dates advanced by approximately the same amount (~5–6 days), with considerable between‐individual variation in the arrival‐breeding interval. The arrival‐breeding interval was shorter for: (a) individuals that arrived later in the season compared to early‐arriving birds, (b) for experienced females compared to first‐year breeders, (c) as spring progressed, and (d) in later years compared to earlier ones. The influence of these factors was much larger for birds arriving earlier in the season compared to later arriving birds, with most effects on variation in the arrival‐breeding interval being absent in late‐arriving birds. Thus, in this population it appears that the timing of breeding is not constrained by arrival for early‐ to midarriving birds, but instead is dependent on local conditions after arrival. For late‐arriving birds, however, the timing of breeding appears to be influenced by arrival constraints. Hence, impacts of climate change on arrival dates and local conditions are expected to vary for different parts of the population, with potential negative impacts associated with these factors likely to differ for early‐ versus late‐arriving birds.     

Role of phenotypic plasticity and population differentiation in adaptation to novel environmental conditions

Species can adapt to new environmental conditions either through individual phenotypic plasticity, intraspecific genetic differentiation in adaptive traits, or both. Wild emmer wheat, Triticum dicoccoides, an annual grass with major distribution in Eastern Mediterranean region, is predicted to experience in the near future, as a result of global climate change, conditions more arid than in any part of the current species distribution. To understand the role of the above two means of adaptation, and the effect of population range position, we analyzed reaction norms, extent of plasticity, and phenotypic selection across two experimental environments of high and low water availability in two core and two peripheral populations of this species. We studied 12 quantitative traits, but focused primarily on the onset of reproduction and maternal investment, which are traits that are closely related to fitness and presumably involved in local adaptation in the studied species. We hypothesized that the population showing superior performance under novel environmental conditions will either be genetically differentiated in quantitative traits or exhibit higher phenotypic plasticity than the less successful populations. We found the core population K to be the most plastic in all three trait categories (phenology, reproductive traits, and fitness) and most successful among populations studied, in both experimental environments; at the same time, the core K population was clearly genetically differentiated from the two edge populations. Our results suggest that (1) two means of successful adaptation to new environmental conditions, phenotypic plasticity and adaptive genetic differentiation, are not mutually exclusive ways of achieving high adaptive ability; and (2) colonists from some core populations can be more successful in establishing beyond the current species range than colonists from the range extreme periphery with conditions seemingly closest to those in the new environment.     

Phenotypic plasticity and divergence in gene expression

The extent to which phenotypic plasticity, or the ability of a single genotype to produce different phenotypes in different environments, impedes or promotes genetic divergence has been a matter of debate within evolutionary biology for many decades (see, for example, Ghalambor et al. 2007 ; Pfennig et al. 2010 ). Similarly, the role of evolution in shaping phenotypic plasticity remains poorly understood (Pigliucci 2005 ). In this issue of Molecular Ecology, Dayan et al. ( 2015 ) provide empirical data relevant to these questions by assessing the extent of plasticity and divergence in the expression levels of 2272 genes in muscle tissue from killifish (genus Fundulus) exposed to different temperatures. F. heteroclitus (Fig.  1 A) and F. grandis are minnows that inhabit estuarine marshes (Fig.  1 B) along the coasts of the Atlantic Ocean and Gulf of Mexico in North America. These habitats undergo large variations in temperature both daily and seasonally, and these fish are known to demonstrate substantial phenotypic plasticity in response to temperature change (e.g. Fangue et al. 2006 ). Furthermore, the range of F. heteroclitus spans a large latitudinal gradient of temperatures, such that northern populations experience temperatures that are on average ~10°C colder than do southern populations (Schulte 2007 ). By comparing gene expression patterns between populations of these fish from different thermal habitats held in the laboratory at three different temperatures, Dayan et al. ( 2015 ) address two important questions regarding the interacting effects of plasticity and evolution: (i) How does phenotypic plasticity affect adaptive divergence? and (ii) How does adaptive divergence affect plasticity?     

Rainfall-induced changes in food availability modify the spring departure programme of a migratory bird

Climatic warming has intensified selection for earlier reproduction in many organisms, but potential constraints imposed by climate change outside the breeding period have received little attention. Migratory birds provide an ideal model for exploring such constraints because they face warming temperatures on temperate breeding grounds and declining rainfall on many tropical non-breeding areas. Here, we use longitudinal data on spring departure dates of American redstarts (Setophaga ruticilla) to show that annual variation in tropical rainfall and food resources are associated with marked change in the timing of spring departure of the same individuals among years. This finding challenges the idea that photoperiod alone regulates the onset of migration, providing evidence that intensifying drought in the tropical winter could hinder adaptive responses to climatic warming in the temperate zone.     

表型可塑性与外来植物的入侵能力

外来植物的入侵能力与其性状之间的关系是入侵生态学中的基本问题之一。成功的入侵种常常能占据多样化的生境,并以广幅的环境耐受性为特征。遗传分化(包括生态型分化)和表型可塑性是广布性物种适应变化、异质性生境的两种不同但并不矛盾和排斥的策略。越来越多的实验证据表明,表型可塑性具有确定的遗传基础,本身是一种可以独立进化的性状。许多入侵种遗传多样性比较低,但同时又占据了广阔的地理分布区和多样化的生境,表型可塑性可能在这些物种的入侵成功和随后的扩散中起到了关键作用。本文首先介绍表型可塑性的含义,简述表型可塑性和生物适应的关系,然后从理论分析和实验证据两个方面论述了表型可塑性与外来植物入侵能力的相关性,最后针对进一步的研究工作进行了讨论。当然,并非所有入侵种的成功都能归因于表型可塑性,作者认为对于那些遗传多样性比较低同时又占据多样化生境的入侵种,表型可塑性和入侵能力的正相关可能是一条普遍法则,而非特例。     

Phenotypic plasticity in gene expression contributes to divergence of locally adapted populations of Fundulus heteroclitus

We examine the interaction between phenotypic plasticity and evolutionary adaptation using muscle gene expression levels among populations of the fish Fundulus heteroclitus acclimated to three temperatures. Our analysis reveals shared patterns of phenotypic plasticity due to thermal acclimation as well as non‐neutral patterns of variation among populations adapted to different thermal environments. For the majority of significant differences in gene expression levels, phenotypic plasticity and adaptation operate on different suites of genes. The subset of genes that demonstrate both adaptive differences and phenotypic plasticity, however, exhibit countergradient variation of expression. Thus, expression differences among populations counteract environmental effects, reducing the phenotypic differentiation between populations. Finally, gene‐by‐environment interactions among genes with non‐neutral patterns of expression suggest that the penetrance of adaptive variation depends on the environmental conditions experienced by the individual.