Climate warming: a loss of variation in populations can accompany reproductive shifts

The most documented response of organisms to climate warming is a change in the average timing of seasonal activities (phenology). Although we know that these average changes can differ among species and populations, we do not know whether climate warming impacts within‐population variation in phenology. Using data from five study sites collected during a 13‐year survey, we found that the increase in spring temperatures is associated with a reproductive advance of 10 days in natural populations of common lizards (Zootoca vivipara). Interestingly, we show a correlated loss of variation in reproductive dates within populations. As illustrated by a model, this shortening of the reproductive period can have significant negative effects on population dynamics. Consequently, we encourage tests in other species to assess the generality of decreased variation in phenological responses to climate change.     

Direct and indirect selection on flowering time,water‐use efficiency (WUE, δ13C), and WUE plasticity to drought in Arabidopsis thaliana

Flowering time and water-use efficiency (WUE) are two ecological traits that are important for plant drought response. To understand the evolutionary significance of natural genetic variation in flowering time, WUE, and WUE plasticity to drought in Arabidopsis thaliana, we addressed the following questions: (1) How are ecophysiological traits genetically correlated within and between different soil moisture environments? (2) Does terminal drought select for early flowering and drought escape? (3) Is WUE plasticity to drought adaptive and/or costly? We measured a suite of ecophysiological and reproductive traits on 234 spring flowering accessions of A. thaliana grown in well-watered and season-ending soil drying treatments, and quantified patterns of genetic variation, correlation, and selection within each treatment. WUE and flowering time were consistently positively genetically correlated. WUE was correlated with WUE plasticity, but the direction changed between treatments. Selection generally favored early flowering and low WUE, with drought favoring earlier flowering significantly more than well-watered conditions. Selection for lower WUE was marginally stronger under drought. There were no net fitness costs of WUE plasticity. WUE plasticity (per se) was globally neutral, but locally favored under drought. Strong genetic correlation between WUE and flowering time may facilitate the evolution of drought escape, or constrain independent evolution of these traits. Terminal drought favored drought escape in these spring flowering accessions of A. thaliana. WUE plasticity may be favored over completely fixed development in environments with periodic drought.     

Assortative mating by flowering time and its effect on correlated traits in variable environments

Reproductive timing is a key life‐history trait that impacts the pool of available mates, the environment experienced during flowering, and the expression of other traits through genetic covariation. Selection on phenology, and its consequences on other life‐history traits, has considerable implications in the context of ongoing climate change and shifting growing seasons. To test this, we grew field‐collected seed from the wildflower Mimulus guttatus in a greenhouse to assess the standing genetic variation for flowering time and covariation with other traits. We then created full‐sib families through phenological assortative mating and grew offspring in three photoperiod treatments representing seasonal variation in daylength. We find substantial quantitative genetic variation for the onset of flowering time, which covaried with vegetative traits. The assortatively‐mated offspring varied in their critical photoperiod by over two hours, so that families differed in their probability of flowering across treatments Allocation to flowering and vegetative growth changed across the daylength treatments, with consistent direction and magnitude of covariation among flowering time and other traits. Our results suggest that future studies of flowering time evolution should consider the joint evolution of correlated traits and shifting seasonal selection to understand how environmental variation influences life histories.     

Response to joint selection on germination and flowering phenology depends on the direction of selection

Flowering and germination time are components of phenology, a complex phenotype that incorporates a number of traits. In natural populations, selection is likely to occur on multiple components of phenology at once. However, we have little knowledge of how joint selection on several phenological traits influences evolutionary response. We conducted one generation of artificial selection for all combinations of early and late germination and flowering on replicated lines within two independent base populations in the herb Campanula americana. We then measured response to selection and realized heritability for each trait. Response to selection and heritability were greater for flowering time than germination time, indicating greater evolutionary potential of this trait. Selection for earlier phenology, both flowering and germination, did not depend on the direction of selection on the other trait, whereas response to selection to delay germination and flowering was greater when selection on the other trait was in the opposite direction (e.g., early germination and late flowering), indicating a negative genetic correlation between the traits. Therefore, the extent to which correlations shaped response to selection depended on the direction of selection. Furthermore, the genetic correlation between timing of germination and flowering varies across the trait distributions. The negative correlation between germination and flowering time found when selecting for delayed phenology follows theoretical predictions of constraint for traits that jointly determine life history schedule. In contrast, the lack of constraint found when selecting for an accelerated phenology suggests a reduction of the covariance due to strong selection favoring earlier flowering and a shorter life cycle. This genetic architecture, in turn, will facilitate further evolution of the early phenology often favored in warm climates.     

No geographic variation in thermoregulatory colour plasticity and limited variation in heat‐avoidance behaviour in Battus philenor caterpillars

Phenotypic plasticity can help organisms cope with variation in their current environment, including temperature variation, but not all environments are equally variable. In the least variable or extreme environments, plasticity may no longer be used. In this case, the plasticity could be lost altogether, or it could persist with either the same or an altered reaction norm, depending on factors such as the plasticity's costs. In the pipevine swallowtail caterpillar (Battus philenor), I tested for changes in two forms of heat‐avoidance plasticity, colour change and refuge‐seeking behaviour, across the species’ range in the United states, including the cooler eastern parts of its range where colour change has not been observed and is unlikely to be needed. I found that both heat‐avoidance behaviour and colour change persisted in all surveyed populations. Indeed, the reaction norm for colour change remained nearly unaltered, whereas the threshold for refuge‐seeking only changed slightly across populations. These results suggest that the costs of these plastic traits are low enough for them to be maintained by whatever minimal gene flow the population receives. I show that plasticity can be maintained unaltered in populations where it is not used and discuss the potential consequences of this persistence for both the ecology and evolution of plasticity.     

Phenology and phenotypic natural selection on the flowering time of a deceit-pollinated tropical orchid, Myrmecophila christinae

BACKGROUND AND AIMS: Flowering phenology is described and the effect of flowering time on pollination success is evaluated in the deceit-pollinated tropical orchid, Myrmecophila christinae. It was expected that, due to this species' deceit pollination strategy and low observed pollinator visit rate, there would be a higher probability of natural selection events favouring individuals flowering away from the population flowering peak. METHODS: The study covers two consecutive years and four populations of M. christinae located along the north coast of the Yucatán Peninsula. For phenological and pollination success data, a total of 110 individuals were monitored weekly in 1998, and 83 individuals in 1999, during all the flowering and fruiting season. KEY RESULTS: The results showed significant differences in the probability of donating and receiving pollen throughout the flowering season. The probability of receiving or donating pollen increased the further an individual flowering was from the flowering peak. Regression analysis showed directional and disruptive phenotypic natural selection gradients, suggesting the presence of selection events unfavourable to flowering during flowering peak, for both male success (pollen removal) and female success (fruit production). However, the intensity and significance of the natural selection events varied between populations from year to year. The variation between seasons and populations was apparently due to variations in the density of reproductive individuals in each population and each season. CONCLUSIONS: As in other deceit-pollinated orchids, natural selection in M. christinae favours individuals flowering early or late in relation to population peak flowering. However, results also suggested a fluctuating regime of selective events act on flowering time of M. christinae.     

Climate variation alters the synchrony of host–parasitoid interactions

Observed changes in mean temperature and increased frequency of extreme climate events have already impacted the distributions and phenologies of various organisms, including insects. Although some research has examined how parasitoids will respond to colder temperatures or experimental warming, we know relatively little about how increased variation in temperature and humidity could affect interactions between parasitoids and their hosts. Using a study system consisting of emerald ash borer (EAB), Agrilus planipennis, and its egg parasitoid Oobius agrili, we conducted environmentally controlled laboratory experiments to investigate how increased seasonal climate variation affected the synchrony of host–parasitoid interactions. We hypothesized that increased climate variation would lead to decreases in host and parasitoid survival, host fecundity, and percent parasitism (independent of host density), while also influencing percent diapause in parasitoids. EAB was reared in environmental chambers under four climate variation treatments (standard deviations in temperature of 1.24, 3.00, 3.60, and 4.79°C), while O. agrili experiments were conducted in the same environmental chambers using a 4 × 3 design (four climate variation treatments × 3 EAB egg densities). We found that EAB fecundity was negatively associated with temperature variation and that temperature variation altered the temporal egg laying distribution of EAB. Additionally, even moderate increases in temperature variation affected parasitoid emergence times, while decreasing percent parasitism and survival. Furthermore, percent diapause in parasitoids was positively associated with humidity variation. Our findings indicate that relatively small changes in the frequency and severity of extreme climate events have the potential to phenologically isolate emerging parasitoids from host eggs, which in the absence of alternative hosts could lead to localized extinctions. More broadly, these results indicate how climate change could affect various life history parameters in insects, and have implications for consumer–resource stability and biological control.     

Phenotypic integration in an extended phenotype: among‐individual variation in nest‐building traits of the alfalfa leafcutting bee (Megachile rotundata)

Structures such as nests and burrows are an essential component of many organisms’ life‐cycle and require a complex sequence of behaviours. Because behaviours can vary consistently among individuals and be correlated with one another, we hypothesized that these structures would (1) show evidence of among‐individual variation, (2) be organized into distinct functional modules and (3) show evidence of trade‐offs among functional modules due to limits on energy budgets. We tested these hypotheses using the alfalfa leafcutting bee, Megachile rotundata, a solitary bee and important crop pollinator. Megachile rotundata constructs complex nests by gathering leaf materials to form a linear series of cells in pre‐existing cavities. In this study, we examined variation in the following nest construction traits: reproduction (number of cells per nest and nest length), nest protection (cap length and number of leaves per cap), cell construction (cell size and number of leaves per cell) and cell provisioning (cell mass) from 60 nests. We found a general decline in investment in cell construction and provisioning with each new cell built. In addition, we found evidence for both repeatability and plasticity in cell provisioning with little evidence for trade‐offs among traits. Instead, most traits were positively, albeit weakly, correlated (r ~ 0.15), and traits were loosely organized into covarying modules. Our results show that individual differences in nest construction are detectable at a level similar to that of other behavioural traits and that these traits are only weakly integrated. This suggests that nest components are capable of independent evolutionary trajectories.     

Antagonistic species interaction drives selection for sex in a predator–prey system

The evolutionary maintenance of sexual reproduction has long challenged biologists as the majority of species reproduce sexually despite inherent costs. Providing a general explanation for the evolutionary success of sex has thus proven difficult and resulted in numerous hypotheses. A leading hypothesis suggests that antagonistic species interaction can generate conditions selecting for increased sex due to the production of rare or novel genotypes that are beneficial for rapid adaptation to recurrent environmental change brought on by antagonism. To test this ecology‐based hypothesis, we conducted experimental evolution in a predator (rotifer)–prey (algal) system by using continuous cultures to track predator–prey dynamics and in situ rates of sex in the prey over time and within replicated experimental populations. Overall, we found that predator‐mediated fluctuating selection for competitive versus defended prey resulted in higher rates of genetic mixing in the prey. More specifically, our results showed that fluctuating population sizes of predator and prey, coupled with a trade‐off in the prey, drove the sort of recurrent environmental change that could provide a benefit to sex in the prey, despite inherent costs. We end with a discussion of potential population genetic mechanisms underlying increased selection for sex in this system, based on our application of a general theoretical framework for measuring the effects of sex over time, and interpreting how these effects can lead to inferences about the conditions selecting for or against sexual reproduction in a system with antagonistic species interaction.     

When directional selection reduces geographic variation in traits mediating species interactions

Although we often focus on the causes of geographic variation, understanding processes that act to reduce geographic variation is also important. Here, we consider a process whereby adaptive foraging across the landscape and directional selection exerted by a conifer seed predator, the common crossbill (Loxia curvirostra), potentially act to homogenize geographic variation in the defensive traits of its prey. We measured seed predation and phenotypic selection exerted by crossbills on black pine (Pinus nigra) at two sites in the Pindos Mountains, Greece. Seed predation by crossbills was over an order of magnitude higher at the site where cone scale thickness was significantly thinner, which was also the cone trait that was the target of selection at the high predation site. Additional comparisons of selection differentials demonstrate that crossbills exert selection on black pine that is consistent in form across space and time, and increases in strength with increasing seed predation. If predators distribute themselves in relation to the defensive traits of their prey and the strength of selection predators exert is proportional to the amount of predation, then predators may act to homogenize trait variation among populations of their prey in a process analogous to coevolutionary alternation with escalation.     

Phenotypic selection on flowering phenology and pollination efficiency traits between Primula populations with different pollinator assemblages

Floral traits have largely been attributed to phenotypic selection in plant–pollinator interactions. However, the strength of this link has rarely been ascertained with real pollinators. We conducted pollinator observations and estimated selection through female fitness on flowering phenology and floral traits between two Primula secundiflora populations. We quantified pollinator‐mediated selection by subtracting estimates of selection gradients of plants receiving supplemental hand pollination from those of plants receiving open pollination. There was net directional selection for an earlier flowering start date at populations where the dominant pollinators were syrphid flies, and flowering phenology was also subjected to stabilized quadratic selection. However, a later flowering start date was significantly selected at populations where the dominant pollinators were legitimate (normal pollination through the corolla tube entrance) and illegitimate bumblebees (abnormal pollination through nectar robbing hole which located at the corolla tube), and flowering phenology was subjected to disruptive quadratic selection. Wider corolla tube entrance diameter was selected at both populations. Furthermore, the strength of net directional selection on flowering start date and corolla tube entrance diameter was stronger at the population where the dominant pollinators were syrphid flies. Pollinator‐mediated selection explained most of the between‐population variations in the net directional selection on flowering phenology and corolla tube entrance diameter. Our results suggested the important influence of pollinator‐mediated selection on floral evolution. Variations in pollinator assemblages not only resulted in variation in the direction of selection but also the strength of selection on floral traits.     

Evolutionary stasis despite selection on a heritable trait in an invasive zooplankton

Invasive species are one of the greatest threats to ecosystems, and there is evidence that evolution plays an important role in the success or failure of invasions. Yet, few studies have measured natural selection and evolutionary responses to selection in invasive species, particularly invasive animals. We quantified the strength of natural selection on the defensive morphology (distal spine) of an invasive zooplankton, Bythotrephes longimanus, in Lake Michigan across multiple months during three growing seasons. We used multiple lines of evidence, including historic and contemporary wild‐captured individuals and palaeoecology of retrieved spines, to assess phenotypic change in distal spine length since invasion. We found evidence of temporally variable selection, with selection for decreased distal spine length early in the growing season and selection for increased distal spine length later in the season. This trend in natural selection is consistent with seasonal changes in the relative strength of non‐gape‐limited and gape‐limited fish predation. Yet, despite net selection for increased distal spine length and a known genetic basis for distal spine length, we observed little evidence of an evolutionary response to selection. Multiple factors likely limit an evolutionary response to selection, including genetic correlations, trade‐offs between components of fitness, and phenotypic plasticity.     

Drought affects the coordination of belowground and aboveground resource‐related traits in Solidago canadensis in China

Quantifying patterns of variation and coordination of plant functional traits can help to understand the mechanisms underlying both invasiveness and adaptation of plants. Little is known about the coordinated variations of performance and functional traits of different organs in invasive plants, especially in response to their adaptation to environmental stressors. To identify the responses of the invasive species Solidago canadensis to drought, 180 individuals were randomly collected from 15 populations and 212 ramets were replanted in a greenhouse to investigate both the response and coordination between root and leaf functional traits. Drought significantly decreased plant growth and most of the root and leaf functional traits, that is, root length, surface area, volume and leaf size, number, and mass fraction, except for the root length ratio and root mass fraction. Phenotypic plasticity was higher in root traits than in leaf traits in response to drought, and populations did not differ significantly. The plasticity of most root functional traits, that is, root length (RL), root surface area (RSA), root volume (RV), and root mass fraction (RMF), were significantly positively correlated with biomass between control and drought. However, the opposite was found for leaf functional traits, that is, specific leaf area (SLA), leaf area ratio (LAR), and leaf mass fraction (LMF). Drought enhanced the relationship between root and leaf, that is, 26 pairwise root–leaf traits were significantly correlated under drought, while only 15 pairwise root–leaf traits were significantly correlated under control conditions. Significant correlations were found between biomass and all measured functional traits except for leaf size. RV, root length ratio, RMF, total area of leaves, and LMF responded differently to water availability. These responses enable S. canadensis to cope with drought conditions and may help to explain the reason of the vast ecological amplitude of this species.     

Herbivory and natural selection on flowering phenology in wild sunflower, Helianthus annuus

Plant fitness is strongly affected by flowering phenology, and there are several ecological factors that are thought to shape the distribution of flowering times. One relatively underexamined factor is the timing and intensity of attack by herbivores that feed on flowers or developing seeds. This study tests the hypothesis that herbivores that feed on developing seeds of wild sunflower, Helianthus annuus (Asteraceae), impose selection on flowering phenology. First, the study population was found to contain genetic variation for mean date of flowering, so this trait could evolve if natural selection were operating. Next, the phenological pattern of abundance of five seed-feeding herbivores was documented. Damage by three herbivores, Haplorhynchites aeneus (Cucurlionidae), the head-clipping weevil, Homoeosoma electellum (Lepidoptera: Pyralidae), the sunflower moth, and Suleima helianthana (Lepidoptera: Tortricidae), the sunflower bud moth, was highest early in the flowering season, and declined as the season progressed. Damage by one herbivore, the seed fly Gymnocarena diffusa (Diptera: Tephrididae), was lowest early in the flowering season and increased as the season progressed. Finally, damage by two seed weevils, Smicronyx fulvus and S. sordidus (Curculionidae), whose damage was not distinguished, was constant through the flowering period. Third, damage by Haplorhynchites, Homoeosoma, and Suleima was found to be detrimental to plant fitness, suggesting that plants that flower when these herbivores are not abundant should have higher fitness. Finally, two phenotypic selection analyses were performed. The first included damage by Homoeosoma and Suleima, as well as flowering date, leaf area, and inflorescence diameter, as characters predicting plant fitness. In this analysis directional selection was found to act to decrease damage by the two herbivores, but did not act on flowering date. The second selection analysis was identical except that damage by the two herbivores was not included. In this analysis significant directional selection was found to favor later-flowering plants. Comparison of these two analyses suggests that all selection on flowering phenology is attributable to damage by Homoeosoma and Suleima: plants that flower later avoid damage by these two herbivores. While other influences on flowering phenology, such as pollination, mate availability, and seasonality, have been well documented, this study is one of few to demonstrate natural selection on flowering phenology that is a direct consequence of insect attack. Received: 17 November 1998 / Accepted: 18 July 1999     

Colonisation of toxic environments drives predictable life‐history evolution in livebearing fishes (Poeciliidae)

New World livebearing fishes (family Poeciliidae) have repeatedly colonised toxic, hydrogen sulphide‐rich waters across their natural distribution. Physiological considerations and life‐history theory predict that these adverse conditions should favour the evolution of larger offspring. Here, we examined nine poeciliid species that independently colonised toxic environments, and show that these fishes have indeed repeatedly evolved much larger offspring size at birth in sulphidic waters, thus uncovering a widespread pattern of predictable evolution. However, a second pattern, only indirectly predicted by theory, proved additionally common: a reduction in the number of offspring carried per clutch (i.e. lower fecundity). Our analyses reveal that this secondary pattern represents a mere consequence of a classic life‐history trade‐off combined with strong selection on offspring size alone. With such strong natural selection in extreme environments, extremophile organisms may commonly exhibit multivariate phenotypic shifts even though not all diverging traits necessarily represent adaptations to the extreme conditions.     

Genome‐wide detection of signatures of selection in Korean Hanwoo cattle

The Korean Hanwoo cattle have been intensively selected for production traits, especially high intramuscular fat content. It is believed that ancient crossings between different breeds contributed to forming the Hanwoo, but little is known about the genomic differences and similarities between other cattle breeds and the Hanwoo. In this work, cattle breeds were grouped by origin into four types and used for comparisons: the Europeans (represented by six breeds), zebu (Nelore), African taurine (N'Dama) and Hanwoo. All animals had genotypes for around 680 000 SNPs after quality control of genotypes. Average heterozygosity was lower in Nelore and N'Dama (0.22 and 0.21 respectively) than in Europeans (0.26–0.31, with Shorthorn as outlier at 0.24) and Hanwoo (0.29). Pairwise F_ST analyses demonstrated that Hanwoo are more related to European cattle than to Nelore, with N'Dama in an intermediate position. This finding was corroborated by principal components and unsupervised hierarchical clustering. Using genome‐wide smoothed F_ST, 55 genomic regions potentially under positive selection in Hanwoo were identified. Among these, 29 were regions also detected in previous studies. Twenty‐four regions were exclusive to Hanwoo, and a number of other regions were shared with one or two of the other groups. These regions overlap a number of genes that are related to immune, reproduction and fatty acid metabolism pathways. Further analyses are needed to better characterize the ancestry of the Hanwoo cattle and to define the genes responsible to the identified selection peaks.     

Maternal effects and maternal selection arising from variation in allocation of free amino acid to eggs

Maternal provisioning can have profound effects on offspring phenotypes, or maternal effects, especially early in life. One ubiquitous form of provisioning is in the makeup of egg. However, only a few studies examine the role of specific egg constituents in maternal effects, especially as they relate to maternal selection (a standardized selection gradient reflecting the covariance between maternal traits and offspring fitness). Here, we report on the evolutionary consequences of differences in maternal acquisition and allocation of amino acids to eggs. We manipulated acquisition by varying maternal diet (milkweed or sunflower) in the large milkweed bug, Oncopeltus fasciatus. Variation in allocation was detected by examining two source populations with different evolutionary histories and life‐history response to sunflower as food. We measured amino acids composition in eggs in this 2 × 2 design and found significant effects of source population and maternal diet on egg and nymph mass and of source population, maternal diet, and their interaction on amino acid composition of eggs. We measured significant linear and quadratic maternal selection on offspring mass associated with variation in amino acid allocation. Visualizing the performance surface along the major axes of nonlinear selection and plotting the mean amino acid profile of eggs from each treatment onto the surface revealed a saddle‐shaped fitness surface. While maternal selection appears to have influenced how females allocate amino acids, this maternal effect did not evolve equally in the two populations. Furthermore, none of the population means coincided with peak performance. Thus, we found that the composition of free amino acids in eggs was due to variation in both acquisition and allocation, which had significant fitness effects and created selection. However, although there can be an evolutionary response to novel food resources, females may be constrained from reaching phenotypic optima with regard to allocation of free amino acids.