Sexual dimorphism in phenotypic plasticity and persistence under environmental change: An extension of theory and meta-analysis of current data.

Populations must adapt to environmental changes to remain viable. Both evolution and phenotypic plasticity contribute to adaptation, with plasticity possibly being more important for coping with rapid change. Adaptation is complex in species with separate sexes, as the sexes can differ in the strength or direction of natural selection, the genetic basis of trait variation, and phenotypic plasticity. Many species show sex differences in plasticity, yet how these differences influence extinction susceptibility remains unclear. We first extend theoretical models of population persistence in changing environments and show that persistence is affected by sexual dimorphism for phenotypic plasticity, trait genetic architecture, and sex-specific selection. Our models predict that female-biased adaptive plasticity-particularly in traits with modest-to-low cross-sex genetic correlations-typically promotes persistence, though we also identify conditions where sexually monomorphic or male-biased plasticity promotes persistence. We then perform a meta-analysis of sex-specific plasticity under manipulated thermal conditions. Although examples of sexually dimorphic plasticity are widely observed, systematic sex differences are rare. An exception-cold resistance-is systematically female-biased and represents a trait wherein sexually dimorphic plasticity might elevate population viability in changing environments. We discuss our results in light of debates about the roles of evolution and plasticity in extinction susceptibility.

Temporal specific coevolution of Hsp70 and co-chaperone stv expression in Drosophila melanogaster under selection for heat tolerance.

Heat shock proteins (Hsps) have long been candidates for ecological adaptation given their unequivocal role in mitigating cell damage from heat stress, but linking Hsps to heat tolerance has proven difficult given the complexity of thermal adaptation. Experimental evolution has been utilized to examine direct and correlated responses to selection for increased heat tolerance in Drosophila, often focusing on the major Hsp family Hsp70 and/or the master regulator HSF as a selection response, but rarely on other aspects of the heat shock complex. We examined Hsp70 and co-chaperone stv isoform transcript expression in Australian D. melanogaster lines selected for static heat tolerance, and observed a temporal and stv isoform specific, coordinated transcriptional selection response with Hsp70, suggesting that increased chaperone output accompanied increased heat tolerance. We hypothesize that the coordinated evolutionary response of Hsp70 and stv may have arisen as a correlated response resulting from a shared regulatory hierarchy. Our work highlights the complexity and specificity of the heat shock response in D. melanogaster. The selected lines examined also showed correlated responses for other measures of heat tolerance, and the coevolution of Hsp70 and stv provide new avenues to examine the common mechanisms underpinning direct and correlated phenotypic responses to selection for heat tolerance.

Genetic covariances promote climatic adaptation in Australian Drosophila.

Evolutionary potential for adaptation hinges upon the orientation of genetic variation for traits under selection, captured by the additive genetic variance-covariance matrix (G), as well as the evolutionary stability of G. Yet studies that assess both the stability of G and its alignment with selection are extraordinarily rare. We evaluated the stability of G in three Drosophila melanogaster populations that have adapted to local climatic conditions along a latitudinal cline. We estimated population- and sex-specific G matrices for wing size and three climatic stress-resistance traits that diverge adaptively along the cline. To determine how G affects evolutionary potential within these populations, we used simulations to quantify how well G aligns with the direction of trait divergence along the cline (as a proxy for the direction of local selection) and how genetic covariances between traits and sexes influence this alignment. We found that G was stable across the cline, showing no significant divergence overall, or in sex-specific subcomponents, among populations. G also aligned well with the direction of clinal divergence, with genetic covariances strongly elevating evolutionary potential for adaptation to climatic extremes. These results suggest that genetic covariances between both traits and sexes should significantly boost evolutionary responses to environmental change.

A note on simulating null distributions for G matrix comparisons.

Genetic variances and covariances, summarized in G matrices, are key determinants of the course of adaptive evolution. Consequently, understanding how G matrices vary among populations is critical to answering a variety of questions in evolutionary biology. A method has recently been proposed for generating null distributions of statistics pertaining to differences in G matrices among populations. The general approach facilitated by this method is likely to prove to be very important in studies of the evolution of G. We have identified an issue in the method that will cause it to create null distributions of differences in G matrices that are likely to be far too narrow. The issue arises from the fact that the method as currently used generates null distributions of statistics pertaining to differences in G matrices across populations by simulating breeding value vectors based on G matrices estimated from data, randomizing these vectors across populations, and then calculating null values of statistics from G matrices that are calculated directly from the variances and covariances among randomized vectors. This calculation treats breeding values as quantities that are directly measurable, instead of predicted from G matrices that are themselves estimated from patterns of covariance among kin. The existing method thus neglects a major source of uncertainty in G matrices, which renders it anti-conservative. We first suggest a correction to the method. We then apply the original and modified methods to a very simple instructive scenario. Finally, we demonstrate the use of both methods in the analysis of a real data set.

Quantifying maladaptation during the evolution of sexual dimorphism.

Females and males have distinct trait optima, resulting in selection for sexual dimorphism. However, most traits have strong cross-sex genetic correlations, which constrain evolutionary divergence between the sexes and lead to protracted periods of maladaptation during the evolution of sexual dimorphism. While such constraints are thought to be costly in terms of individual and population fitness, it remains unclear how severe such costs are likely to be. Building upon classical models for the 'cost of selection' in changing environments (sensu Haldane), we derived a theoretical expression for the analogous cost of evolving sexual dimorphism; this cost is a simple function of genetic (co)variances of female and male traits and sex differences in trait optima. We then conducted a comprehensive literature search, compiled quantitative genetic data from a diverse set of traits and populations, and used them to quantify costs of sexual dimorphism in the light of our model. For roughly 90% of traits, costs of sexual dimorphism appear to be modest, and comparable to the costs of fixing one or a few beneficial substitutions. For the remaining traits (approx. 10%), sexual dimorphism appears to carry a substantial cost-potentially orders of magnitude greater than costs of selection during adaptation to environmental changes.

Changes in lipid classes of Drosophila melanogaster in response to selection for three stress traits.

Laboratory selection on environmental stress traits is an evolutionary approach that is informative in the context of understanding stress adaptation. Here we characterize changes in a lipidome of Drosophila melanogaster in lines selected for increased heat (elevated heat knockdown refractoriness), cold (decreased time to recover from chill-coma) and desiccation survival. Selection for desiccation resistance resulted in changes in multiple lipid classes used to characterize a lipidome. This included a decrease in triacylglycerols (TAGs) which is relevant to interpretation of storage lipid levels in previous D. melanogaster desiccation survival selection experiments. Chill-coma recovery rate selection was expected to show extensive changes in lipid classes, but only phosphatidic acids exhibited significant change. Selection for increased heat knockdown resistance resulted in a substantial change in the abundance of a class of lipids (diacylglycerols) which could play a role in mediating the heat shock response or result in an increase in neutral lipid mobilization.

Cross-sex genetic correlations and the evolution of sex-specific local adaptation: Insights from classical trait clines in Drosophila melanogaster.

Natural selection varies widely among locations of a species' range, favoring population divergence and adaptation to local environmental conditions. Selection also differs between females and males, favoring the evolution of sexual dimorphism. Both forms of within-species evolutionary diversification are widely studied, though largely in isolation, and it remains unclear whether environmental variability typically generates similar or distinct patterns of selection on each sex. Studies of sex-specific local adaptation are also challenging because they must account for genetic correlations between female and male traits, which may lead to correlated patterns of trait divergence between sexes, whether or not local selection patterns are aligned or differ between the sexes. We quantified sex-specific divergence in five clinally variable traits in Drosophila melanogaster that individually vary in their magnitude of cross-sex genetic correlation (i.e., from moderate to strongly positive). In all five traits, we observed parallel male and female clines, regardless of the magnitude of their genetic correlation. These patterns imply that parallel spatial divergence of female and male traits is a reflection of sexually concordant directional selection imposed by local environmental conditions. In such contexts, genetic correlations between the sexes promote, rather than constrain, local adaptation to a spatially variable environment.

Best practice data life cycle approaches for the life sciences.

Throughout history, the life sciences have been revolutionised by technological advances; in our era this is manifested by advances in instrumentation for data generation, and consequently researchers now routinely handle large amounts of heterogeneous data in digital formats. The simultaneous transitions towards biology as a data science and towards a 'life cycle' view of research data pose new challenges. Researchers face a bewildering landscape of data management requirements, recommendations and regulations, without necessarily being able to access data management training or possessing a clear understanding of practical approaches that can assist in data management in their particular research domain. Here we provide an overview of best practice data life cycle approaches for researchers in the life sciences/bioinformatics space with a particular focus on 'omics' datasets and computer-based data processing and analysis. We discuss the different stages of the data life cycle and provide practical suggestions for useful tools and resources to improve data management practices.

Genomic Trajectories to Desiccation Resistance: Convergence and Divergence Among Replicate Selected Drosophila Lines.

Adaptation to environmental stress is critical for long-term species persistence. With climate change and other anthropogenic stressors compounding natural selective pressures, understanding the nature of adaptation is as important as ever in evolutionary biology. In particular, the number of alternative molecular trajectories available for an organism to reach the same adaptive phenotype remains poorly understood. Here, we investigate this issue in a set of replicated Drosophila melanogaster lines selected for increased desiccation resistance-a classical physiological trait that has been closely linked to Drosophila species distributions. We used pooled whole-genome sequencing (Pool-Seq) to compare the genetic basis of their selection responses, using a matching set of replicated control lines for characterizing laboratory (lab-)adaptation, as well as the original base population. The ratio of effective population size to census size was high over the 21 generations of the experiment at 0.52-0.88 for all selected and control lines. While selected SNPs in replicates of the same treatment (desiccation-selection or lab-adaptation) tended to change frequency in the same direction, suggesting some commonality in the selection response, candidate SNP and gene lists often differed among replicates. Three of the five desiccation-selection replicates showed significant overlap at the gene and network level. All five replicates showed enrichment for ovary-expressed genes, suggesting maternal effects on the selected trait. Divergence between pairs of replicate lines for desiccation-candidate SNPs was greater than between pairs of control lines. This difference also far exceeded the divergence between pairs of replicate lines for neutral SNPs. Overall, while there was overlap in the direction of allele frequency changes and the network and functional categories affected by desiccation selection, replicates showed unique responses at all levels, likely reflecting hitchhiking effects, and highlighting the challenges in identifying candidate genes from these types of experiments when traits are likely to be polygenic.

A collection of Australian Drosophila datasets on climate adaptation and species distributions.

The Australian Drosophila Ecology and Evolution Resource (ADEER) collates Australian datasets on drosophilid flies, which are aimed at investigating questions around climate adaptation, species distribution limits and population genetics. Australian drosophilid species are diverse in climatic tolerance, geographic distribution and behaviour. Many species are restricted to the tropics, a few are temperate specialists, and some have broad distributions across climatic regions. Whereas some species show adaptability to climate changes through genetic and plastic changes, other species have limited adaptive capacity. This knowledge has been used to identify traits and genetic polymorphisms involved in climate change adaptation and build predictive models of responses to climate change. ADEER brings together 103 datasets from 39 studies published between 1982-2013 in a single online resource. All datasets can be downloaded freely in full, along with maps and other visualisations. These historical datasets are preserved for future studies, which will be especially useful for assessing climate-related changes over time.

Experimental removal of sexual selection leads to decreased investment in an immune component in female Tribolium castaneum.

Because of divergent selection acting on males and females arising from different life-history strategies, polyandry can be expected to promote sexual dimorphism of investment into immune function. In previous work we have established the existence of such divergence within populations where males and females are exposed to varying degrees of polyandry. We here test whether the removal of sexual selection via enforced monogamy generates males and females that have similar levels of investment in immune function. To test this prediction experimentally, we measured differences between the sexes in a key immune measurement (phenoloxidase (PO) activity) and resistance to the microsporidian Paranosema whitei in Tribolium castaneum lines that evolved under monogamous (sexual selection absent) vs polyandrous (sexual selection present) mating systems. At generation 49, all selected lines were simultaneously assessed for PO activity and resistance to their natural parasite P. whitei after two generations of relaxed selection. We found that the polyandrous regime was associated with a clear dimorphism in immune function: females had significantly higher PO activities than males in these lines. In contrast, there was no such difference between the sexes in the lines evolving under the monogamous regime. Survival in the infection experiment did not differ between mating systems or sexes. Removing sexual selection via enforced monogamy thus seems to erase intersexual differences in immunity investment. We suggest that higher PO activities in females that have evolved under sexual selection might be driven by the increased risk of infections and/or injuries associated with exposure to multiple males.

Multifarious selection through environmental change: acidity and predator-mediated adaptive divergence in the moor frog (Rana arvalis).

Environmental change can simultaneously cause abiotic stress and alter biological communities, yet adaptation of natural populations to co-changing environmental factors is poorly understood. We studied adaptation to acid and predator stress in six moor frog (Rana arvalis) populations along an acidification gradient, where abundance of invertebrate predators increases with increasing acidity of R. arvalis breeding ponds. First, we quantified divergence among the populations in anti-predator traits (behaviour and morphology) at different rearing conditions in the laboratory (factorial combinations of acid or neutral pH and the presence or the absence of a caged predator). Second, we evaluated relative fitness (survival) of the populations by exposing tadpoles from the different rearing conditions to predation by free-ranging dragonfly larvae. We found that morphological defences (relative tail depth) as well as survival of tadpoles under predation increased with increasing pond acidity (under most experimental conditions). Tail depth and larval size mediated survival differences among populations, but the contribution of trait divergence to survival was strongly dependent on prior rearing conditions. Our results indicate that R. arvalis populations are adapted to the elevated predator pressure in acidified ponds and emphasize the importance of multifarious selection via both direct (here: pH) and indirect (here: predators) environmental changes.

Genetic isolation by environment or distance: which pattern of gene flow is most common?

Gene flow among populations can enhance local adaptation if it introduces new genetic variants available for selection, but strong gene flow can also stall adaptation by swamping locally beneficial genes. These outcomes can depend on population size, genetic variation, and the environmental context. Gene flow patterns may align with geographic distance (IBD--isolation by distance), whereby immigration rates are inversely proportional to the distance between populations. Alternatively gene flow may follow patterns of isolation by environment (IBE), whereby gene flow rates are higher among similar environments. Finally, gene flow may be highest among dissimilar environments (counter-gradient gene flow), the classic "gene-swamping" scenario. Here we survey relevant studies to determine the prevalence of each pattern across environmental gradients. Of 70 studies, we found evidence of IBD in 20.0%, IBE in 37.1%, and both patterns in 37.1%. In addition, 10.0% of studies exhibited counter-gradient gene flow. In total, 74.3% showed significant IBE patterns. This predominant IBE pattern of gene flow may have arisen directly through natural selection or reflect other adaptive and nonadaptive processes leading to nonrandom gene flow. It also precludes gene swamping as a widespread phenomenon. Implications for evolutionary processes and management under rapidly changing environments (e.g., climate change) are discussed.

Assessing the relative importance of environmental effects, carry-over effects and species differences in thermal stress resistance: a comparison of Drosophilids across field and laboratory generations.

There is increasing interest in comparing species of related organisms for their susceptibility to thermal extremes in order to evaluate potential vulnerability to climate change. Comparisons are typically undertaken on individuals collected from the field with or without a period of acclimation. However, this approach does not allow the potential contributions of environmental and carry-over effects across generations to be separated from inherent species differences in susceptibility. To assess the importance of these different sources of variation, we here considered heat and cold resistance in Drosophilid species from tropical and temperate sites in the field and across two laboratory generations. Resistance in field-collected individuals tended to be lower when compared with F1 and F2 laboratory generations, and species differences in field flies were only weakly correlated to differences established under controlled rearing conditions, unlike in F1-F2 comparisons. This reflected large environmental effects on resistance associated with different sites and conditions experienced within sites. For the 8 h cold recovery assay there was no strong evidence of carry-over effects, whereas for the heat knockdown and 2 h cold recovery assays there was some evidence for such effects. However, for heat these were species specific in direction. Variance components for inherent species differences were substantial for resistance to heat and 8 h cold stress, but small for 2 h cold stress, though this may be a reflection of the species being considered in the comparisons. These findings highlight that inherent differences among species are difficult to characterise accurately without controlling for environmental sources of variation and carry-over effects. Moreover, they also emphasise the complex nature of carry-over effects that vary depending on the nature of stress traits and the species being evaluated.

Are there genetic trade-offs between immune and reproductive investments in Tribolium castaneum?

Parasites impose strong selection on hosts to defend themselves, which is expected to result in trade-offs with other fitness traits such as reproduction. Here we test for genetic trade-offs between reproductive traits and immunity using Tribolium castaneum lines that were subject to experimental evolution. The lines have been exposed to contrasting sexual selection intensities via different sex ratios (female-biased, equal and male-biased). After 56 generations, the lines have significantly diverged and those experiencing high sexual selection have evolved males who are superior competitors for reproductive success, and females who are more resistant to multiple mating. All selected lines were assessed for both an immune measurement (phenoloxidase (PO) activity) and host resistance to the microsporidian Nosema whitei after two generations of relaxed selection. In contrast to our expectations we did not find any evidence for a genetic trade-off between investment in reproduction and immunity. Both PO and Nosema resistance did not differ between lines, despite their divergences in reproductive investment due to variation in sexual selection and conflict. Nevertheless, overall we found that females had higher PO activities and in the Nosema free control treatment survived longer than males, suggesting that females generally invest more in PO and survival under control conditions than males. This result fits the Bateman's principle, which states that females gain fitness through increased immunity and longevity, while males gain fitness through increased mating success.

Adaptive divergence in moor frog (Rana arvalis) populations along an acidification gradient: inferences from Q(st) -F(st) correlations.

Microevolutionary responses to spatial variation in the environment seem ubiquitous, but the relative role of selection and neutral processes in driving phenotypic diversification remain often unknown. The moor frog (Rana arvalis) shows strong phenotypic divergence along an acidification gradient in Sweden. We here used correlations among population pairwise estimates of quantitative trait (P(ST) or Q(ST) from common garden estimates of embryonic acid tolerance and larval life-history traits) and neutral genetic divergence (F(ST) from neutral microsatellite markers), as well as environmental differences (pond pH, predator density, and latitude), to test whether this phenotypic divergence is more likely due to divergent selection or neutral processes. We found that trait divergence was more strongly correlated with environmental differences than the neutral marker divergence, suggesting that divergent natural selection has driven phenotypic divergence along the acidification gradient. Moreover, pairwise P(ST) s of embryonic acid tolerance and Q(ST) s of metamorphic size were strongly correlated with breeding pond pH, whereas pairwise Q(ST) s of larval period and growth rate were more strongly correlated with geographic distance/latitude and predator density, respectively. We suggest that incorporating measurements of environmental variation into Q(ST) -F(ST) studies can improve our inferential power about the agents of natural selection in natural populations.

Adaptive divergence of the moor frog (Rana arvalis) along an acidification gradient.

BACKGROUND: Environmental stress can result in strong ecological and evolutionary effects on natural populations, but to what extent it drives adaptive divergence of natural populations is little explored. We used common garden experiments to study adaptive divergence in embryonic and larval fitness traits (embryonic survival, larval growth, and age and size at metamorphosis) in eight moor frog, Rana arvalis, populations inhabiting an acidification gradient (breeding pond pH 4.0 to 7.5) in southwestern Sweden. Embryos were raised until hatching at three (pH 4.0, 4.3 and 7.5) and larvae until metamorphosis at two (pH 4.3 and 7.5) pH treatments. To get insight into the putative selective agents along this environmental gradient, we measured relevant abiotic and biotic environmental variables from each breeding pond, and used linear models to test for phenotype-environment correlations. RESULTS: We found that acid origin populations had higher embryonic and larval acid tolerance (survival and larval period were less negatively affected by low pH), higher larval growth but slower larval development rates, and metamorphosed at a larger size. The phenotype-environment correlations revealed that divergence in embryonic acid tolerance and metamorphic size correlated most strongly with breeding pond pH, whereas divergence in larval period and larval growth correlated most strongly with latitude and predator density, respectively. CONCLUSION: Our results suggest that R. arvalis has diverged in response to pH mediated selection along this acidification gradient. However, as latitude and pH were closely spatially correlated in this study, further studies are needed to disentangle the specific agents of natural selection along acidification gradients. Our study highlights the need to consider the multiple interacting selective forces that drive adaptive divergence of natural populations along environmental stress gradients.