Buffer Environmental Variation Research Articles

Niche Construction Affects the Variability and Strength of Natural Selection.

Consideration of the properties of the sources of selection potentially helps biologists account for variation in selection. Here we explore how the variability of natural selection is affected by organisms that regulate the experienced environment through their activities (whether by constructing components of their local environments, such as nests, burrows, or pupal cases, or by choosing suitable resources). Specifically, we test the predictions that organism-constructed sources of selection that buffer environmental variation will result in (i) reduced variation in selection gradients, including reduced variation between (a) years (temporal variation) and (b) locations (spatial variation), and (ii) weaker directional selection relative to nonconstructed sources. Using compiled data sets of 1,045 temporally replicated selection gradients, 257 spatially replicated selection gradients, and a pooled data set of 1,230 selection gradients, we find compelling evidence for reduced temporal variation and weaker selection in response to constructed compared to nonconstructed sources of selection and some evidence for reduced spatial variation in selection. These findings, which remained robust to alternative data sets, taxa, analytical methods, definitions of constructed/nonconstructed, and other tests of reliability, suggest that organism-manufactured or chosen components of environments may have qualitatively different properties from other environmental features.

Trans-generational plasticity in response to immune challenge is constrained by heat stress.

Trans‐generational plasticity (TGP) is the adjustment of phenotypes to changing habitat conditions that persist longer than the individual lifetime. Fitness benefits (adaptive TGP) are expected upon matching parent–offspring environments. In a global change scenario, several performance‐related environmental factors are changing simultaneously. This lowers the predictability of offspring environmental conditions, potentially hampering the benefits of TGP. For the first time, we here explore how the combination of an abiotic and a biotic environmental factor in the parental generation plays out as trans‐generational effect in the offspring. We fully reciprocally exposed the parental generation of the pipefish Syngnathus typhle to an immune challenge and elevated temperatures simulating a naturally occurring heatwave. Upon mating and male pregnancy, offspring were kept in ambient or elevated temperature regimes combined with a heat‐killed bacterial epitope treatment. Differential gene expression (immune genes and DNA‐ and histone‐modification genes) suggests that the combined change of an abiotic and a biotic factor in the parental generation had interactive effects on offspring performance, the temperature effect dominated over the immune challenge impact. The benefits of certain parental environmental conditions on offspring performance did not sum up when abiotic and biotic factors were changed simultaneously supporting that available resources that can be allocated to phenotypic trans‐generational effects are limited. Temperature is the master regulator of trans‐generational phenotypic plasticity, which potentially implies a conflict in the allocation of resources towards several environmental factors. This asks for a reassessment of TGP as a short‐term option to buffer environmental variation in the light of climate change.

Heat shock protein 83 plays pleiotropic roles in embryogenesis, longevity, and fecundity of the pea aphid Acyrthosiphon pisum

Heat shock protein 83 (HSP83) is homologous to the chaperone HSP90. It has pleiotropic functions in Drosophila melanogaster, including the control of longevity and fecundity, and facilitates morphological evolution by buffering cryptic deleterious mutations in wild populations. In the pea aphid Acyrthosiphon pisum, HSP83 expression is moderately induced by bacterial infection but upregulated more strongly in response to heat stress and fungal infection. Stress-inducible heat shock proteins are of considerable evolutionary and ecological importance because they are known to buffer environmental variation and to influence fitness under non-optimal conditions. To investigate the functions of HSP83 in viviparous aphids, we used RNA interference to attenuate its expression and studied the impact on complex parameters. The RNA interference (RNAi)-mediated depletion of HSP83 expression in A. pisum reduced both longevity and fecundity, suggesting this chaperone has an evolutionarily conserved function in insects. Surprisingly, HSP83 depletion reduced the number of viviparous offspring while simultaneously increasing the number of premature nymphs developing in the ovaries, suggesting an unexpected role in aphid embryogenesis and eclosion. The present study indicates that reduced HSP83 expression in A. pisum reveals both functional similarities and differences compared with its reported roles in holometabolous insects. Its impact on aphid lifespan, fecundity, and embryogenesis suggests a function that determines their fitness. This could be achieved by targeting different client proteins, recruiting distinct co-chaperones or transposon activation.

Moving south: effects of water temperatures on the larval development of invasive cane toads (Rhinella marina) in cool-temperate Australia.

The distributional limits of many ectothermic species are set by thermal tolerances of early‐developmental stages in the life history; embryos and larvae often are less able to buffer environmental variation than are conspecific adults. In pond‐breeding amphibians, for example, cold water may constrain viability of eggs and larvae, even if adults can find suitable thermal conditions in terrestrial niches. Invasive species provide robust model systems for exploring these questions, because we can quantify thermal challenges at the expanding range edge (from field surveys) and larval responses to thermal conditions (in the laboratory). Our studies on invasive cane toads (Rhinella marina) at the southern (cool‐climate) edge of their expanding range in Australia show that available ponds often average around 20°C during the breeding period, 10°C lower than in many areas of the toads’ native range, or in the Australian tropics. Our laboratory experiments showed that cane toad eggs and larvae cannot develop successfully at 16°C, but hatching success and larval survival rates were higher at 20°C than in warmer conditions. Lower temperatures slowed growth rates, increasing the duration of tadpole life, but also increased metamorph body mass. Water temperature also influenced metamorph body shape (high temperatures reduced relative limb length, head width, and body mass) and locomotor performance (increased speed from intermediate temperatures, longer hops from high temperatures). In combination with previous studies, our data suggest that lower water temperatures may enhance rather than reduce recruitment of cane toads, at least in areas where pond temperatures reach or exceed 20°C. That condition is fulfilled over a wide area of southern Australia, suggesting that the continuing expansion of this invasive species is unlikely to be curtailed by the impacts of relatively low water temperatures on the viability of early life‐history stages.

Modelling the effects of variation in reproductive traits on fish population resilience

Abstract Preserving larger fish is often advocated as a conservation measure to help fish populations buffer environmental variation and fishing pressure. The rationale is that several size- and age-dependent reproductive traits confer a higher reproductive value to larger fish. The effects of variation in these reproductive traits on the dynamics of populations under various fishing patterns are however seldom evaluated. In this study, we develop a simulation model to evaluate how variation in three reproductive traits (fecundity–mass, hatching probability, and batch spawning) impacts the capacity of a fish population to withstand and recover from high fishing pressure. Biological functions of the model were calibrated based on the Gulf of Maine Atlantic cod stock, which is currently experiencing its lowest biomass level ever estimated. Results showed that variation in the shape of the fecundity–mass relationship had the most substantial impact on population resistance and recovery. Batch spawning and variation in hatching probability had limited impacts. Furthermore, results showed that preserving larger fish by imposing a slot fishery increased the resistance of the population to high fishing pressure, because it helped preserve the population reproductive potential determined by the high fecundity of large fish. The slot fishery, however, impeded population recovery, because it distributed the fishing pressure on intermediate-size classes which potential for biomass growth is maximal. This study underlines the importance of using precise size-dependent fecundity estimates when evaluating the productivity and sustainability of fisheries, as well as the importance of identifying priority among the components of population resilience (e.g. resistance or recovery) before implementing size-selective harvest strategies.

Vanishing Chromosomal Inversion Clines inDrosophila subobscurafrom Chile: Is Behavioral Thermoregulation to Blame?

Chromosomal inversion clines paralleling the long-standing ones in native Palearctic populations of Drosophila subobscura evolved swiftly after this species invaded the Americas in the late 1970s and early 1980s. However, the new clines did not consistently continue to converge on the Old World baseline. Our recent survey of Chilean populations of D. subobscura shows that inversion clines have faded or even changed sign with latitude. Here, we investigate the hypothesis that this fading of inversion clines might be due to the Bogert effect, namely, that flies' thermoregulatory behavior has eventually compensated for environmental variation in temperature, thus buffering selection on thermal-related traits. We show that latitudinal divergence in thermal preference (Tp) has evolved in Chile for females, with higher-latitude flies having a lower mean Tp. Plastic responses in Tp also lessen latitudinal thermal variation because flies developed at colder temperatures prefer warmer microclimates. Our results are consistent with the idea that active behavioral thermoregulation might buffer environmental variation and reduce the potential effect of thermal selection on other traits as chromosomal arrangements.

A Gene's Ability to Buffer Variation Is Predicted by Its Fitness Contribution and Genetic Interactions

BackgroundMany single-gene knockouts result in increased phenotypic (e.g., morphological) variability among the mutant's offspring. This has been interpreted as an intrinsic ability of genes to buffer genetic and environmental variation. A phenotypic capacitor is a gene that appears to mask phenotypic variation: when knocked out, the offspring shows more variability than the wild type. Theory predicts that this phenotypic potential should be correlated with a gene's knockout fitness and its number of negative genetic interactions. Based on experimentally measured phenotypic capacity, it was suggested that knockout fitness was unimportant, but that phenotypic capacitors tend to be hubs in genetic and physical interaction networks.Methodology/Principal FindingsWe re-analyse the available experimental data in a combined model, which includes knockout fitness and network parameters as well as expression level and protein length as predictors of phenotypic potential. Contrary to previous conclusions, we find that the strongest predictor is in fact haploid knockout fitness (responsible for 9% of the variation in phenotypic potential), with an additional contribution from the genetic interaction network (5%); once these two factors are taken into account, protein-protein interactions do not make any additional contribution to the variation in phenotypic potential.Conclusions/SignificanceWe conclude that phenotypic potential is not a mysterious “emergent” property of cellular networks. Instead, it is very simply determined by the overall fitness reduction of the organism (which in its compromised state can no longer compensate for multiple factors that contribute to phenotypic variation), and by the number (and presumably nature) of genetic interactions of the knocked-out gene. In this light, Hsp90, the prototypical phenotypic capacitor, may not be representative: typical phenotypic capacitors are not direct “buffers” of variation, but are simply genes encoding central cellular functions.

The quantitative genetics of phenotypic robustness.

Phenotypic robustness, or canalization, has been extensively investigated both experimentally and theoretically. However, it remains unknown to what extent robustness varies between individuals, and whether factors buffering environmental variation also buffer genetic variation. Here we introduce a quantitative genetic approach to these issues, and apply this approach to data from three species. In mice, we find suggestive evidence that for hundreds of gene expression traits, robustness is polymorphic and can be genetically mapped to discrete genomic loci. Moreover, we find that the polymorphisms buffering genetic variation are distinct from those buffering environmental variation. In fact, these two classes have quite distinct mechanistic bases: environmental buffers of gene expression are predominantly sex-specific and trans-acting, whereas genetic buffers are not sex-specific and often cis-acting. Data from studies of morphological and life-history traits in plants and yeast support the distinction between polymorphisms buffering genetic and environmental variation, and further suggest that loci buffering different types of environmental variation do overlap with one another. These preliminary results suggest that naturally occurring polymorphisms affecting phenotypic robustness could be abundant, and that these polymorphisms may generally buffer either genetic or environmental variation, but not both.

Evidence that Fold-Change, and Not Absolute Level, of β-Catenin Dictates Wnt Signaling

In response to Wnt stimulation, beta-catenin accumulates and activates target genes. Using modeling and experimental analysis, we found that the level of beta-catenin is sensitive to perturbations in the pathway, such that cellular variation would be expected to alter the signaling outcome. One unusual parameter was robust: the fold-change in beta-catenin level (post-Wnt/pre-Wnt). In Xenopus, dorsal-anterior development and target gene expression are robust to perturbations that alter the final level but leave the fold-change intact. These suggest, first, that despite cellular noise, the cell responds reliably to Wnt stimulation by maintaining a robust fold-change in beta-catenin. Second, the transcriptional machinery downstream of the Wnt pathway does not simply read the beta-catenin level after Wnt stimulation but computes fold-changes in beta-catenin. Analogous to Weber's Law in sensory physiology, some gene transcription networks must respond to fold-changes in signals, rather than absolute levels, which may buffer stochastic, genetic, and environmental variation.

Network Hubs Buffer Environmental Variation in Saccharomyces cerevisiae

Regulatory and developmental systems produce phenotypes that are robust to environmental and genetic variation. A gene product that normally contributes to this robustness is termed a phenotypic capacitor. When a phenotypic capacitor fails, for example when challenged by a harsh environment or mutation, the system becomes less robust and thus produces greater phenotypic variation. A functional phenotypic capacitor provides a mechanism by which hidden polymorphism can accumulate, whereas its failure provides a mechanism by which evolutionary change might be promoted. The primary example to date of a phenotypic capacitor is Hsp90, a molecular chaperone that targets a large set of signal transduction proteins. In both Drosophila and Arabidopsis, compromised Hsp90 function results in pleiotropic phenotypic effects dependent on the underlying genotype. For some traits, Hsp90 also appears to buffer stochastic variation, yet the relationship between environmental and genetic buffering remains an important unresolved question. We previously used simulations of knockout mutations in transcriptional networks to predict that many gene products would act as phenotypic capacitors. To test this prediction, we use high-throughput morphological phenotyping of individual yeast cells from single-gene deletion strains to identify gene products that buffer environmental variation in Saccharomyces cerevisiae. We find more than 300 gene products that, when absent, increase morphological variation. Overrepresented among these capacitors are gene products that control chromosome organization and DNA integrity, RNA elongation, protein modification, cell cycle, and response to stimuli such as stress. Capacitors have a high number of synthetic-lethal interactions but knockouts of these genes do not tend to cause severe decreases in growth rate. Each capacitor can be classified based on whether or not it is encoded by a gene with a paralog in the genome. Capacitors with a duplicate are highly connected in the protein–protein interaction network and show considerable divergence in expression from their paralogs. In contrast, capacitors encoded by singleton genes are part of highly interconnected protein clusters whose other members also tend to affect phenotypic variability or fitness. These results suggest that buffering and release of variation is a widespread phenomenon that is caused by incomplete functional redundancy at multiple levels in the genetic architecture.

Tuber size variation and organ preformation constrain growth responses of a spring geophyte

Functional responses to environmental variation do not only depend on the genetic potential of a species to express different trait values, but can also be limited by characteristics, such as the timing of organ (pre-) formation, aboveground longevity or the presence of a storage organ. In this experiment we tested to what degree variation in tuber size and organ preformation constrain the responsiveness to environmental quality and whether responsiveness is modified by the availability of stored resources by exposing the spring geophyte Bunium bulbocastanum to different light and nutrient regimes. Growth and biomass partitioning were affected by initial tuber size and resource availability. On average, tuber weight amounted to 60%, but never less than 30% of the total plant biomass. Initial tuber size, considered an estimate of the total carbon pool available at the onset of treatments, affected plant growth and reproduction throughout the experiment but had little effect on the responsiveness of plants to the treatments. The responsiveness was partly constrained by organ preformation: in the second year variation of leaf number was considerably larger than in the first year of the treatments. The results indicate that a spring geophyte with organ preformation has only limited possibilities to respond to short-term fluctuations of the environment, as all leaves and the inflorescence are preformed in the previous growing season and resources stored in tubers are predominantly used for survival during dormancy and are not invested into plastic adjustments to environmental quality. Such spring geophytes have only limited possibilities to buffer environmental variation. This explains their restriction to habitats characterized by predictable changes of the environmental conditions.

THE DYNAMICS OF PLANT POPULATIONS: DOES THE HISTORY OF INDIVIDUALS MATTER?

Historical events have been used to explain a wide range of phenomena including geographical distributions of species, community diversity, and population structure. At the level of individuals, historical effects in which past conditions influence future performance are particularly likely to occur in long-lived organisms that store resources between seasons and that form organs months or years before their elaboration. Such carry-over mechanisms have been documented in several perennial plant species, but the implications for population processes are poorly known. In this study, I examine how the history of individuals influences their future performance, population dynamics, and life cycle structure in the long-lived herb Lathyrus vernus. Overall effects of plant history on population dynamics, in terms of growth rate, reproductive values, stable stage distribution, and elasticities, are examined by comparing an ordinary first-order matrix model with a second-order matrix model. In the latter, not only the present state of individuals, but also their past state is allowed to influence future fate. The results demonstrate that the history of individuals is sometimes important in models of population dynamics. Plant size change over a one-year period was negatively correlated among time intervals. Addition of the previous year's stage in population models shifted the growth rate from positive (λ = 1.010) to negative (λ = 0.986) and increased the proportion of small established individuals in the stable stage distribution. If historical effects are due to a capacity to buffer environmental variation and regain size or state, as in L. vernus, then recruitment contributes less and stasis more to population growth than suggested by ahistorical models. The presence of historical effects at the level of individuals, in any form, may have important consequences for population development and should be included in any interpretation of the life-cycle structure.

Aspects of the Cryobiology of the Intertidal Harpacticoid CopepodTigriopus brevicornis(O. F. Müller)

Cold-resistance studies of marine invertebrates have concentrated on intertidal sedentary organisms, which are often subjected to subzero air temperatures in winter. Mobile rock pool inhabitants have been rarely studied because such habitats are thought to buffer environmental variation. However, it is not uncommon for small upper-shore rock pools (∼2 by 1 cm) to become completely frozen. Such supralittoral habitats are subject to extreme physicochemical fluctuations especially in salinity (0 to 300‰) and temperature (−1 to +32°C) due to evaporation and dilution. The dominant invertebrate in such habitats is the harpacticoid copepodTigriopus brevicornis.Aspects of the cryobiology ofT. brevicorniswere investigated using differential scanning calorimetry (DSC). Thermograms obtained from DSC allowed determinations of freeze-onset (supercooling point, SCP), melt-onset, and melt-peak (melting point, MP) temperatures, together with estimation of the proportion of water freezing in the samples. The effects of acclimation salinity, temperature, starvation, and reproductive state on these cryobiological parameters were investigated. Acclimation to increasing salinity depressed the SCP, with the highest salinity (70‰) producing the lowest SCP, melt-onset, and MP temperatures at −27.5, −15.2, and −9.5°C respectively. The highest acclimation temperature (20°C) produced the lowest SCP (−23.4°C). Starvation significantly increased the SCP, melt-onset, and MP temperatures in comparison to fed individuals acclimated to the same salinity. The presence of eggs or ovaries in individual copepods elevated the SCP compared to nongravid females and males. LT50studies showed that acclimation to high salinity improved the ability ofT. brevicornisto survive in frozen seawater. Seventy parts per thousand acclimated individuals had an LT50of 64.9 h compared with just 1.4 h for 5‰ acclimated individuals in frozen seawater at −5°C. The study shows that the cold-resistance capabilities ofT. brevicorniscan be affected by several different factors, and the link between the osmoconforming nature of this species and its cold resistance is discussed.

Variation and covariation among life-history traits in Rumex acetosella from a successional old-field gradient.

In this study morphological variation and the potential for competition to affect biomass and seedling selection of the families of five populations of Rumex acetosella L. sampled along a successional old-field gradient have been investigated. Seeds from 25 families were submitted to four competitive regimes: no competition (one plant per pot), medium competition (two plants/ pot taking plants from the same population), high within-population competition (four individuals from the same population in a pot) and high between-population competition (four individuals from two different populations in a pot). Eight traits were analysed after 3 months of growth for variation among families within populations. A significant difference among families within the two older populations was recorded for sexual biomass and related components. High sensitivity of these traits to density was observed in all populations except the youngest, suggesting specialization to particular environmental conditions in late successional populations, and a good adaptive capacity to buffer environmental variation in the pioneer population. Little significant interaction between competitive regimes and families within populations was found, i.e. genotypes within each population showed little variation in their response to environmental variation. Genotypic variance decreased with increasing competitive conditions for the majority of the traits. However, the percentage of variance in sexual reproduction explained by family was stable among treatments. Tradeoffs between vegetative reproduction and sexual reproduction were recorded at the population level along the successional gradient, with increasing competitive conditions. As succession proceeds, we observed a decrease in sexual reproduction and an increase in vegetative reproduction. At the family level, correlation among traits were similar when plants were grown in the absence of competition and at high density, with a significant negative correlation between sexual reproduction and vegetative reproduction. For both sprout number and sexual biomass, the performance of families grown under all the treatments was positively correlated. Together these results indicate allocational constraints on the reproductive biology of R. acetosella that may be favoured by natural selection and have influenced population differentiation along the successional gradient. However, they also revealed that the potential exists for evolutionary specialization through plasticity, in response to variation in environmental conditions.