High Altitude Frogs (Rana kukonoris) Adopt a Diversified Bethedging Strategy in the Face of Environmental Unpredictability

Environmental unpredictability can influence strategies of maternal investment among eggs within a clutch. Models predict that breeding females should adopt a diversified bet-hedging strategy in unpredictable environments, but empirical field evidence from Asia is scarce. Here we tested this hypothesis by exploring spatial patterns in egg size along an altitudinal gradient in a frog species(Rana kukunoris) inhabiting the Tibetan Plateau. Within-clutch variability in egg size increased as the environment became variable(e.g., lower mean monthly temperature and mean monthly rainfall at higher altitudes), and populations in environments with more unpredictable rainfall produced eggs that were smaller and more variable in size. We provide support for a diversified bet-hedging strategy in high-altitude environments, which experience dynamic weather patterns and therefore are of unpredictable environmental quality. This strategy may be an adaptive response to lower environmental quality and higher unpredictable environmental variance. Such a strategy should increase the likelihood of breeding success and maximize maternal lifetime fitness by producing offspring that are adapted to current environmental conditions. We speculate that in high-altitude environments prone to physical disturbance, breeding females are unable to consistently produce the optimal egg size due to physiological constraints imposed by environmental conditions(e.g., duration of the active season, food availability). Species and populations whose breeding strategies are adapted to cope with uncertain environmental conditions by adjusting offspring size and therefore quality show a remarkable degree of ability to cope with future climatic changes.     

Designing artificial selection experiments for specific objectives

The observed genetic gain (ΔP) from selection in a finite population is the possible expected genetic gain E(Δ G) minus the difference in inbreeding depression effects in the selected and control lines. The inbreeding depression can be avoided by crossing the control and selected ♂ and ♀ parents to unrelated mates and summing the observed gains. The possible expected gain will be reduced by an amount D from the predicted gain because of the effects of the genetic limit and random genetic drift, the magnitude of which is a function of effective population size, N. The expected value of D is zero in unselected control populations and in the first generation for selected populations. Therefore, this source of bias can be reduced by increasing N in the selected populations and can be avoided by selecting for a single generation. To obtain observed responses which are unbiased estimates of the predicted response from which to estimate the realized heritability (or regression) in the zero generation, or to test genetic theory based on infinite population size, single-generation selection with many replications would be most efficient. To measure the "total" effect or genetic efficiency of a selection criterion or method, including the effect of different selection intensities, effective population sizes, and space requirements, more than one generation of selection is required to estimate the expected response in breeding values. The efficiency, in the sense of minimum variance, of estimating the expected breeding values at any generation t will decline as the number of generations t increases. The variance of either the estimated mean gain or the regression of gain on selection differential can be reduced more by increasing the number of replicates K than by increasing the number of generations t. Also the general pattern of the response over t can be estimated if the N's are known. Therefore, two- or not more than three-generation selection experiments with many replications would be most efficient.     

Habitat‐driven life history variation in an amphibian metapopulation

Life‐history theory states that, during the lifetime of an individual, resources are allocated to either somatic maintenance or reproduction. Resource allocation tradeoffs determine the evolution and ecology of life‐history strategies and determine an organisms’ position along the fast–slow continuum. Theory predicts that environmental stochasticity is an important driver of resource allocation and therefore life‐history evolution. Highly stochastic environments are expected to increase uncertainty in reproductive success and select for iteroparity and a slowing down of the life history. To date, most empirical studies have used comparisons among species to examine these theoretical predictions. By contrast, few have investigated how environmental stochasticity affects life‐history strategies at the intraspecific level. In this study, we examined how variation in breeding site stochasticity (among‐year variability in pond volume and hydroperiod) promotes the co‐occurrence of different life‐history strategies in a spatially structured population, and determines life‐history position along the fast–slow continuum in the yellow‐bellied toad Bombina variegata. We collected mark–recapture data from a metapopulation and used multievent capture–recapture models to estimate survival, recruitment and breeding probabilities. We found higher survival and longer lifespans in populations inhabiting variable sites compared to those breeding in stable ones. In addition, probabilities of recruitment and skipping a breeding event were higher in variable sites. The temporal variance of survival and recruitment probabilities, as well as the probability to skip breeding, was higher in variable sites. Taken together, these findings indicate that populations breeding in variable sites experienced a slowing down of the life‐history. Our study thus revealed similarities in the macroevolutionary and microevolutionary processes shaping life‐history evolution.     

Experimental evidence for the adaptive value of sexual reproduction

It is generally believed that recombination by sexual reproduction is unfavourable in constant environments but is of adaptive value under changing environmental conditions. To test this theory, experimental populations of yeast (Saccharomyces cerevisiae) were set up and maintained at different levels of environmental heterogeneity. Recombination was estimated by determining sporulation rates. Sporulation rates first increased in populations living in highly variable environments, but after some time began to decrease. The decrease started last and was slowest in populations which were maintained under the same conditions for a sufficiently long time, to allow some adaptation of the gene pool to the respective environment. Patterns of genotypic variability could not be interpreted in such simple terms, but there was a statistically significant correlation between sporulation rate and genotypic variability. This correlation is to be expected because recombination generates genotypic variability. Summing up, recombination by sexual reproduction is advantageous in changing environments if the population can track the changes in the environment by changing its genotypic structure.     

Evolution in a changing environment: a case study with great tit fledging mass

Heritable phenotypic traits under significant and consistent directional selection often fail to show the expected evolutionary response. A potential explanation for this contradiction is that because environmental conditions change constantly, environmental change can mask an evolutionary response to selection. We combined an "animal model" analysis with 36 years of data from a long-term study of great tits (Parus major) to explore selection on and evolution of a morphological trait: body mass at fledging. We found significant heritability of this trait, but despite consistent positive directional selection on both the phenotypic and the additive genetic component of body mass, the population mean phenotypic value declined rather than increased over time. However, the mean breeding value for body mass at fledging increased over time, presumably in response to selection. We show that the divergence between the response to selection observed at the levels of genotype and phenotype can be explained by a change in environmental conditions over time, that is, related both to increased spring temperature before breeding and elevated population density. Our results support the suggestion that measuring phenotypes may not always give a reliable impression of evolutionary trajectories and that understanding patterns of phenotypic evolution in nature requires an understanding of how the environment has itself changed.     

The max bin regression method to identify maximum bioindicator responses to ecological drivers

A need in environmental science is to determine the response range of a bioindicator to environmental drivers. A common problem with regression based approaches is the indicator response may be obfuscated by many zero or low-value observations when the organisms are not present because of life history characteristics. A method is described for determining the maximum response of an ecological variable to environmental drivers using a median approach. A regression is performed on the relationship histogram after taking the maximum ecological response value from a set of evenly spaced bins. This technique is an alternative to quantile regression at the 95% level and is analyzed on general examples and specific applications in coastal ecology using benthic macroinfauna as bioindicators. This new technique is useful for ecosystem management purposes where the maximum response of a biological indicator to an environmental driver is desired and is analogous to determining the ‘area under the curve’ of a regression.     

Selection for egg production on part records

Summary Responses from four generations of index selection for egg production to 280 days of age in four White Leghorn populations have been presented. A pedigreed randombred population derived from one of the lines was reared with the selected lines to measure the environmental trend. The magnitude of total as well as average response although varying from population to population was positive in all the lines studied. Close correspondence between predicted and realized gains indicated that natural selection, genotype environmental interactions and environmental fluctuations were unimportant during the course of selection. Realized heritabilities agreed fairly well with the estimated heritabilities in at least three out of four populations studied. Probable reasons for variable and insufficient response were investigated.     

An empirical demonstration of risk-sensitive foraging preferences

We report laboratory experiments with yellow-eyed juncos (Junco phaeonotus) revealing that the birds' foraging preferences for variable rewards respond not only to the mean, but also the variance, of food rewards. The nature of their preferences for variable rewards is related to their expected daily energy budget. We summarize the birds' preferences in utility functions for energetic rewards. Since mean reward size is inadequate to predict their behaviour, we believe that foraging models should consider environmental stochasticity and an animal's response to this variation.     

The influence of multiple inseminations and multiple foundresses on social evolution

The breeding biology of a population determines the way in which individuals are distributed within and between progeny groups and, thus, affects the genetic variation within and between these groups. The breeding biology of any organism can be characterized by the distribution of the numbers of mates of females, the apportionment of paternity among males, the distribution of the numbers of females reproducing in common nests, and the apportionment of total fecundity within a nest among founding females. In addition, the possibility of genetic correlations among mates or among founding females is an important consideration and will be addressed in a later paper. The influence of the breeding biology on social evolution was evaluated by deriving the necessary conditions for the spread of genes for social behaviors and the rate of spread of these genes for populations with different breeding biologies. The first step in this derivation is to demonstrate that selection for genes determining social behavior can be represented as the covariance between gene frequency and relative fitness. Secondly, it is shown that this covariance can be formally partitioned into within and between group components. Thirdly, each covariance component is shown to be equivalent to the product of a genetic variance and a coefficient of linear regression of relative fitness on gene frequency. Lastly, specific models for the genotype fitnesses and breeding biologies are assumed and the necessary conditions for the increase in the frequency of altruistic alleles are obtained. The theory illustrates that variation in the numbers of mates per female has less of an effect on the evolution of social behaviors than does variation in the numbers of reproductive females per nest. In addition, it points out that the harmonic mean number of mates per female or of females per nest is a more useful summary statistic for characterizing populations with respect to the expected degree of evolved sociality than is the arithmetic mean.     

Developmental thermal plasticity among Drosophila melanogaster populations

Many biotic and abiotic variables influence the dispersal and distribution of organisms. Temperature has a major role in determining these patterns because it changes daily, seasonally and spatially, and these fluctuations have a significant impact on an organism's behaviour and fitness. Most ecologically relevant phenotypes that are adaptive are also complex and thus they are influenced by many underlying loci that interact with the environment. In this study, we quantified the degree of thermal phenotypic plasticity within and among populations by measuring chill‐coma recovery times of lines reared from egg to adult at two different environmental temperatures. We used sixty genotypes from six natural populations of Drosophila melanogaster sampled along a latitudinal gradient in South America. We found significant variation in thermal plasticity both within and among populations. All populations exhibit a cold acclimation response, with flies reared at lower temperatures having increased resistance to cold. We tested a series of environmental parameters against the variation in population mean thermal plasticity and discovered the mean thermal plasticity was significantly correlated with altitude of origin of the population. Pairing our data with previous experiments on viability fitness assays in the same populations in fixed and variable environments suggests an adaptive role of this thermal plasticity in variable laboratory environments. Altogether, these data demonstrate abundant variation in adaptive thermal plasticity within and among populations.     

Consequences of the genetic threshold model for observing partial migration under climate change scenarios

Migration is a widespread phenomenon across the animal kingdom as a response to seasonality in environmental conditions. Partially migratory populations are populations that consist of both migratory and residential individuals. Such populations are very common, yet their stability has long been debated. The inheritance of migratory activity is currently best described by the threshold model of quantitative genetics. The inclusion of such a genetic threshold model for migratory behavior leads to a stable zone in time and space of partially migratory populations under a wide range of demographic parameter values, when assuming stable environmental conditions and unlimited genetic diversity. Migratory species are expected to be particularly sensitive to global warming, as arrival at the breeding grounds might be increasingly mistimed as a result of the uncoupling of long‐used cues and actual environmental conditions, with decreasing reproduction as a consequence. Here, we investigate the consequences for migratory behavior and the stability of partially migratory populations under five climate change scenarios and the assumption of a genetic threshold value for migratory behavior in an individual‐based model. The results show a spatially and temporally stable zone of partially migratory populations after different lengths of time in all scenarios. In the scenarios in which the species expands its range from a particular set of starting populations, the genetic diversity and location at initialization determine the species’ colonization speed across the zone of partial migration and therefore across the entire landscape. Abruptly changing environmental conditions after model initialization never caused a qualitative change in phenotype distributions, or complete extinction. This suggests that climate change‐induced shifts in species’ ranges as well as changes in survival probabilities and reproductive success can be met with flexibility in migratory behavior at the species level, which will reduce the risk of extinction.     

Evolution of metabolic rate in a parasitic wasp: the role of limitation in intrinsic resources

Metabolic rate, a physiological trait closely related to fitness traits, is expected to evolve in response to two main environmental variables: (1) climate, low metabolic rates being found in dry and hot regions when comparing populations originating from different climates in a common garden experiment and (2) resource limitations, low metabolic rates being selected when resources are limited. The main goal of this study was to investigate if differences in intrinsic resource limitations may have disrupted the expected evolution of metabolic rate in response to climate in a parasitic wasp. We compared CO(2) production of females from 4 populations of a Drosophila parasitoid, Leptopilina boulardi, as an estimate of their metabolic rate. Two populations from a hot and dry area able to synthesise lipids de novo at adult stage were compared with two populations originating from a mild and humid climate where no lipid accumulation during adult life was observed. These last females are thus more limited in lipids than the first ones. We observed that a high metabolic rate has been selected in hot and dry environments, contrarily to the results of a great majority of studies. We suggest that lipogenesis occurring there may have allowed the selection of a higher metabolic rate, as females are less limited in energetic resources than females from the mild environment. A high metabolic rate may have been selected there as it partly compensates for the long distances that females have to cross to find laying opportunities in distant orchards. We suggest that intrinsic resources should be integrated when investigating geographical variations in metabolism as this factor may disrupt evolution in response to climate.     

Understanding landscape patterns of temporal variability in avian populations to improve environmental impact assessments

It is recognized that wildlife populations exhibit spatial and temporal variability in patterns of species richness across heterogeneous landscapes. This phenomenon can prove problematic for environmental practitioners when attempting to complete comprehensive environmental assessments (EAs) with limited field surveys. A better understanding of regional spatio-temporal patterns in population dynamics should enhance site-level decision-making. In this study, the variability of seasonal data across the Credit River Watershed, southern Ontario, is assessed for a hierarchy of conservation measures including species richness, and two conservation wildlife response guilds based on primary habitat and area sensitivity. Bird populations were monitored at 24 forest monitoring plots across the watershed by the authors twice a season from 2003 to 2010 following the protocol of Environment Canada's Forest Bird Monitoring Program. The monitoring plots are located within four land management zones identified as 1) urban, 2) transitional, 3) escarpment and 4) rural. Data from the monitoring program are used to compare species richness among plots across the watershed and among land management zones. In addition, the variability of records from each plot over the 8 year period was determined by means of the Coefficient of Variation (CV) statistic. The mean variability of these records at each site within each land management zone was determined in order to assess whether the temporal variability of bird records might affect the integrity of short term assessments. Finally, a one-way ANOVA was applied to learn whether the result of short-term assessments may be further compounded by differences in the response of selected bird guilds to landscape heterogeneity. The results show that there is a significant difference in mean richness of forest birds among the four management zones. The ANOVAs indicate that significant difference is due to the temporal variability of a) breeding forest interior birds rather than edge birds or generalist species and b) breeding area sensitive species rather than area non-sensitive species. Recommendations are made that environmental assessments targeting forest interior bird populations need to plan sampling strategies that recognize this variability, especially for sites within the transitional and urban zones. Planning in the transition or urbanizing landscape should incorporate landscape ecology principles to sustain current levels of richness in forest species.     

Response to genomic selection: The Bulmer effect and the potential of genomic selection when the number of phenotypic records is limiting

Background

Over the last ten years, genomic selection has developed enormously. Simulations and results on real data suggest that breeding values can be predicted with high accuracy using genetic markers alone. However, to reach high accuracies, large reference populations are needed. In many livestock populations or even species, such populations cannot be established when traits are difficult or expensive to record, or when the population size is small. The value of genomic selection is then questionable.

Methods

In this study, we compare traditional breeding schemes based on own performance or progeny information to genomic selection schemes, for which the number of phenotypic records is limiting. Deterministic simulations were performed using selection index theory. Our focus was on the equilibrium response obtained after a few generations of selection. Therefore, we first investigated the magnitude of the Bulmer effect with genomic selection.

Results

Results showed that the reduction in response due to the Bulmer effect is the same for genomic selection as for selection based on traditional BLUP estimated breeding values, and is independent of the accuracy of selection. The reduction in response with genomic selection is greater than with selection based directly on phenotypes without the use of pedigree information, such as mass selection. To maximize the accuracy of genomic estimated breeding values when the number of phenotypic records is limiting, the same individuals should be phenotyped and genotyped, rather than genotyping parents and phenotyping their progeny. When the generation interval cannot be reduced with genomic selection, large reference populations are required to obtain a similar response to that with selection based on BLUP estimated breeding values based on own performance or progeny information. However, when a genomic selection scheme has a moderate decrease in generation interval, relatively small reference population sizes are needed to obtain a similar response to that with selection on traditional BLUP estimated breeding values.

Conclusions

When the trait of interest cannot be recorded on the selection candidate, genomic selection schemes are very attractive even when the number of phenotypic records is limited, because traditional breeding requires progeny testing schemes with long generation intervals in those cases.     

Correlated response in plasticity to selection for early flowering in Arabidopsis thaliana

Phenotypic plasticity is an important strategy for coping with changing environments. However, environmental change usually results in strong directional selection, and little is known empirically about how this affects plasticity. If genes affecting a trait value also affect its plasticity, selection on the trait should influence plasticity. Synthetic outbred populations of Arabidopsis thaliana were selected for earlier flowering under simulated spring- and winter-annual conditions to investigate the correlated response of flowering time plasticity and its effect on family-by-environment variance (Vg×e) within each selected line. We found that selection affected plasticity in an environmentally dependent manner: under simulated spring-annual conditions, selection increased the magnitude of plastic response but decreased Vg×e; selection under simulated winter-annual conditions reduced the magnitude of plastic response but did not alter Vg×e significantly. As selection may constrain future response to environmental change, the environment for crop breeding and ex situ conservation programmes should be carefully chosen. Models of species persistence under environmental change should also consider the interaction between selection and plasticity.     

A method for simulating patterns of habitat availability at static and dynamic range margins

The dynamics of populations inhabiting range margins are likely to be critically important in determining the response of species to climate change. Despite this, there is a lack of both empirical and theoretical work that examines the behaviour of these populations. Populations living on the edge of a species' range frequently inhabit a more patchily distributed habitat than those that live closer to the centre of the range. This difference is likely to play an important role in determining the dynamics of range margin populations, both when the range is static and when it is dynamic, for example shifting in response to climate change. Here, we present a simple method that simulates the distribution of suitable habitat sites at the edge of a range. Habitat availability is determined as a function of both latitudinal and local environmental variability, and the relative importance of the two can be adjusted. The method is readily extended to describe shifting habitat availability during a period of climate change. We suggest that there is a need for a greater effort to examine the ecology of range margin populations, and believe that the method presented here could be of considerable use in future theoretical studies.     

Investigating connectivity and seasonal differences in wind assistance in the migration of Common Sandpipers

Many migratory bird species have undergone recent population declines, but there is considerable variation in trends between species and between populations employing different migratory routes. Understanding species-specific migratory behaviours is therefore of critical importance for their conservation. The Common Sandpiper Actitis hypoleucos is an Afro-Palaearctic migratory bird species whose European populations are in decline. We fitted geolocators to individuals breeding in England or wintering in Senegal to determine their migration routes and breeding or non-breeding locations. We used these geolocator data in combination with previously published data from Scottish breeding birds to determine the distributions and migratory connectivity of breeding (English and Scottish) and wintering (Senegalese) populations of the Common Sandpiper, and used simulated random migrations to investigate wind assistance during autumn and spring migration. We revealed that the Common Sandpipers tagged in England spent the winter in West Africa, and that at least some birds wintering in Senegal bred in Scandinavia; this provides insights into the links between European breeding populations and their wintering grounds. Furthermore, birds tagged in England, Scotland and Senegal overlapped considerably in their migration routes and wintering locations, meaning that local breeding populations could be buffered against habitat change, but susceptible to large-scale environmental changes. These findings also suggest that contrasting population trends in England and Scotland are unlikely to be the result of population-specific migration routes and wintering regions. Finally, we found that birds used wind to facilitate their migration in autumn, but less so in spring, when the wind costs associated with their migrations were higher than expected at random. This was despite the wind costs of simulated migrations being significantly lower in spring than in autumn. Indeed, theory suggests that individuals are under greater time pressures in spring than in autumn because of the time constraints associated with reproduction.     

Environmental change, phenotypic plasticity, and genetic compensation

When a species encounters novel environmental conditions, some phenotypic characters may develop differently than in the ancestral environment. Most environmental perturbations of development are likely to reduce fitness, and thus selection would usually be expected to favor genetic changes that restore the ancestral phenotype. I propose the term "genetic compensation" to refer to this form of adaptive evolution. Genetic compensation is a subset of genetic accommodation and the reverse of genetic assimilation. When genetic compensation has occurred along a spatial environmental gradient, the mean trait values of populations in different environments may be more similar in the field than when representatives of the same populations are raised in a common environment (i.e., countergradient variation). If compensation is complete, genetic divergence between populations may be cryptic, that is, not detectable in the field. Here I apply the concept of genetic compensation to three examples involving carotenoid-based sexual coloration and then use these and other examples to discuss the concept in a broader context. I show that genetic compensation may lead to a cryptic form of reproductive isolation between populations evolving in different environments, may explain some puzzling cases in which heritable traits exposed to strong directional selection fail to show the expected evolutionary response, and may complicate efforts to monitor populations for signs of environmental deterioration.     

The use of variance in enzyme activity as an indicator of long-term exposure to toxicant-stressed environments in Culex pipiens mosquitoes

1. The identification of easy to use and cheap biomarkers is important as a means of determining whether animals are developing under stressful environmental conditions. Previous studies have indicated that the variance about the mean esterase activity in toxic environments increases in the absence of a significant shift in the mean value, suggesting that variance levels may have potential as a biomarker of toxicant-stressed or otherwise stressful environments.
2. Several field and laboratory populations of the mosquito, Culex pipiens , were examined for esterase activities using a colorimetric assay and levels of polymorphism using polyacrylamide gel electrophoresis. Some of these populations had been exposed to environmental toxicants (organophosphorus (OP) insecticides).
3. The OP-stressed field population had lower levels of polymorphism as indicated by fewer electromorphs than the populations that had not been exposed to OPs. However, the mean level of esterase activity was higher in the OP-stressed populations.
4. Despite having lower genetic variation, the OP-stressed populations showed much higher levels of variation about the mean enzyme activity, at least two orders of magnitude higher, than the unstressed populations. Knowledge of the genetics of OP resistance in these populations confirmed that the increase in variance was not due to the general switching on of genes in response to stress.
5. One field population that had been exposed to heavy metal pollution had similar levels of esterase activity and variation about the mean as the unstressed populations, suggesting that variation only increases in characters directly affected by the environmental pollutant.
6. The probable factors causing the increase in variance and the potential of this type of variation as a biomarker of stressful environments are discussed.     

IS INBREEDING DEPRESSION LOWER IN MALADAPTED POPULATIONS? A QUANTITATIVE GENETICS MODEL

Despite abundant empirical evidence that inbreeding depression varies with both the environment and the genotypic context, theoretical predictions about such effects are still rare. Using a quantitative genetics model, we predict amounts of inbreeding depression for fitness emerging from Gaussian stabilizing selection on some phenotypic trait, on which, for simplicity, genetic effects are strictly additive. Given the strength of stabilizing selection, inbreeding depression then varies simply with the genetic variance for the trait under selection and the distance between the mean breeding value and the optimal phenotype. This allows us to relate the expected inbreeding depression to the degree of maladaptation of the population to its environment. We confront analytical predictions with simulations, in well-adapted populations at equilibrium, as well as in maladapted populations undergoing either a transient environmental shift, or gene swamping in heterogeneous habitats. We predict minimal inbreeding depression in situations of extreme maladaptation. Our model provides a new basis for interpreting experiments that measure inbreeding depression for the same set of genotypes in different environments, by demonstrating that the history of adaptation, in addition to environmental harshness per se, may account for differences in inbreeding depression.