Seedling response to water stress in valley oak (Quercus lobata) is shaped by different gene networks across populations

Drought is a major stress for plants, creating a strong selection pressure for traits that enable plant growth and survival in dry environments. Many drought responses are conserved species‐wide responses, while others vary among populations distributed across heterogeneous environments. We tested how six populations of the widely distributed California valley oak (Quercus lobata) sampled from contrasting climates would differ in their response to soil drying relative to well‐watered controls in a common environment by measuring ecophysiological traits in 93 individuals and gene expression (RNA‐seq) in 42 individuals. Populations did not differ in their adjustment of turgor loss point during soil drying, suggesting a generalized species‐wide response. Differential expression analysis identified 689 genes with a common response to treatment across populations and 470 genes with population‐specific responses. Weighted gene co‐expression network analysis (WGCNA) identified groups of genes with similar expression patterns that may be regulated together (gene modules). Several gene modules responded differently to water stress among populations, suggesting regional differences in gene network regulation. Populations from sites with a high mean annual temperature responded to the imposed water stress with significantly greater changes in gene module expression, indicating that these populations may be locally adapted to respond to drought. We propose that this variation among valley oak populations provides a mechanism for differential tolerance to the increasingly frequent and severe droughts in California.     

VARIATION IN THERMAL PERFORMANCE AND REACTION NORMS AMONG POPULATIONS OF DROSOPHILA MELANOGASTER

The major goal of evolutionary thermal biology is to understand how variation in temperature shapes phenotypic evolution. Comparing thermal reaction norms among populations from different thermal environments allows us to gain insights into the evolutionary mechanisms underlying thermal adaptation. Here, we have examined thermal adaptation in six wild populations of the fruit fly (Drosophila melanogaster) from markedly different natural environments by analyzing thermal reaction norms for fecundity, thorax length, wing area, and ovariole number under ecologically realistic fluctuating temperature regimes in the laboratory. Contrary to expectation, we found only minor differences in the thermal optima for fecundity among populations. Differentiation among populations was mainly due to differences in absolute (and partly also relative) thermal fecundity performance. Despite significant variation among populations in the absolute values of morphological traits, we observed only minor differentiation in their reaction norms. Overall, the thermal reaction norms for all traits examined were remarkably similar among different populations. Our results therefore suggest that thermal adaptation in D. melanogaster predominantly involves evolutionary changes in absolute trait values rather than in aspects of thermal reaction norms.     

Evolution of Drosophila resistance against different pathogens and infection routes entails no detectable maintenance costs

Pathogens exert a strong selective pressure on hosts, entailing host adaptation to infection. This adaptation often affects negatively other fitness‐related traits. Such trade‐offs may underlie the maintenance of genetic diversity for pathogen resistance. Trade‐offs can be tested with experimental evolution of host populations adapting to parasites, using two approaches: (1) measuring changes in immunocompetence in relaxed‐selection lines and (2) comparing life‐history traits of evolved and control lines in pathogen‐free environments. Here, we used both approaches to examine trade‐offs in Drosophila melanogaster populations evolving for over 30 generations under infection with Drosophila C Virus or the bacterium Pseudomonas entomophila, the latter through different routes. We find that resistance is maintained after up to 30 generations of relaxed selection. Moreover, no differences in several classical life‐history traits between control and evolved populations were found in pathogen‐free environments, even under stresses such as desiccation, nutrient limitation, and high densities. Hence, we did not detect any maintenance costs associated with resistance to pathogens. We hypothesize that extremely high selection pressures commonly used lead to the disproportionate expression of costs relative to their actual occurrence in natural systems. Still, the maintenance of genetic variation for pathogen resistance calls for an explanation.     

Adaptive phenotypic divergence in an annual grass differs across biotic contexts*

Climate is a powerful force shaping adaptation within species, yet adaptation to climate occurs against a biotic background: species interactions can filter fitness consequences of genetic variation by altering phenotypic expression of genotypes. We investigated this process using populations of teosinte, a wild annual grass related to maize (Zea mays ssp. mexicana), sampling plants from 10 sites along an elevational gradient as well as rhizosphere biota from three of those sites. We grew half‐sibling teosinte families in each biota to test whether trait divergence among teosinte populations reflects adaptation or drift, and whether rhizosphere biota affect expression of diverged traits. We further assayed the influence of rhizosphere biota on contemporary additive genetic variation. We found that adaptation across environment shaped divergence of some traits, particularly flowering time and root biomass. We also observed that different rhizosphere biota shifted expressed values of these traits within teosinte populations and families and altered within‐population genetic variance and covariance. In sum, our results imply that changes in trait expression and covariance elicited by rhizosphere communities could have played a historical role in teosinte adaptation to environments and that they are likely to play a role in the response to future selection.     

Long‐term acclimation to reciprocal light conditions suggests depth‐related selection in the marine foundation species Posidonia oceanica

Phenotypic differences among populations of the same species reflect selective responses to ecological gradients produced by variations in abiotic and biotic factors. Moreover, they can also originate from genetic differences among populations, due to a reduced gene flow. In this study, we examined the extent of differences in photo‐acclimative traits of Posidonia oceanica (L.) Delile clones collected above and below the summer thermocline (i.e., ?5 and ?25 m) in a continuous population extending along the water depth gradient. During a reciprocal light exposure and subsequent recovery in mesocosms, we assessed degree of phenotypic plasticity and local adaptation of plants collected at different depths, by measuring changes in several traits, such as gene expression of target genes, photo‐physiological features, and other fitness‐related traits (i.e., plant morphology, growth, and mortality rates). Samples were also genotyped, using microsatellite markers, in order to evaluate the genetic divergence among plants of the two depths. Measures collected during the study have shown a various degree of phenotypic changes among traits and experimental groups, the amount of phenotypic changes observed was also dependent on the type of light environments considered. Overall plants collected at different depths seem to be able to acclimate to reciprocal light conditions in the experimental time frame, through morphological changes and phenotypic buffering, supported by the plastic regulation of a reduced number of genes. Multivariate analyses indicated that plants cluster better on the base of their depth origin rather than the experimental light conditions applied. The two groups were genetically distinct, but the patterns of phenotypic divergence observed during the experiment support the hypothesis that ecological selection can play a role in the adaptive divergence of P. oceanica clones along the depth gradient.     

Increased socially mediated plasticity in gene expression accompanies rapid adaptive evolution

Recent theory predicts that increased phenotypic plasticity can facilitate adaptation as traits respond to selection. When genetic adaptation alters the social environment, socially mediated plasticity could cause co‐evolutionary feedback dynamics that increase adaptive potential. We tested this by asking whether neural gene expression in a recently arisen, adaptive morph of the field cricket Teleogryllus oceanicus is more responsive to the social environment than the ancestral morph. Silent males (flatwings) rapidly spread in a Hawaiian population subject to acoustically orienting parasitoids, changing the population's acoustic environment. Experimental altering crickets’ acoustic environments during rearing revealed broad, plastic changes in gene expression. However, flatwing genotypes showed increased socially mediated plasticity, whereas normal‐wing genotypes exhibited negligible expression plasticity. Increased plasticity in flatwing crickets suggests a coevolutionary process coupling socially flexible gene expression with the abrupt spread of flatwing. Our results support predictions that phenotypic plasticity should rapidly evolve to be more pronounced during early phases of adaptation.     

Genetic architecture and phenotypic plasticity of thermally-regulated traits in an eruptive species, <Emphasis Type="Italic">Dendroctonus ponderosae</Emphasis>

Phenotypic plasticity in thermally-regulated traits enables close tracking of changing environmental conditions, and can thereby enhance the potential for rapid population increase, a hallmark of outbreak insect species. In a changing climate, exposure to conditions that exceed the capacity of existing phenotypic plasticity may occur. Combining information on genetic architecture and trait plasticity among populations that are distributed along a latitudinal cline can provide insight into how thermally-regulated traits evolve in divergent environments and the potential for adaptation. Dendroctonus ponderosae feed on Pinus species in diverse climatic regimes throughout western North America, and show eruptive population dynamics. We describe geographical patterns of plasticity in D. ponderosae development time and adult size by examining reaction norms of populations from multiple latitudes. The relative influence of additive and non-additive genetic effects on population differences in the two phenotypic traits at a single temperature is quantified using line-cross experiments and joint-scaling tests. We found significant genetic and phenotypic variation among D. ponderosae populations. Simple additive genetic variance was not the primary source of the observed variation, and dominance and epistasis contributed greatly to the genetic divergence of the two thermally-regulated traits. Hybrid breakdown was also observed in F₂ hybrid crosses between northern and southern populations, further indication of substantial genetic differences among clinal populations and potential reproductive isolation within D. ponderosae. Although it is unclear what maintains variation in the life-history traits, observed plasticity in thermally-regulated traits that are directly linked to rapid numerical change may contribute to the outbreak nature of D. ponderosae, particularly in a changing climate.     

Loci under selection during multiple range expansions of an invasive plant are mostly population specific,but patterns are associated with climate

Identifying the genes underlying rapid evolutionary changes, describing their function and ascertaining the environmental pressures that determine fitness are the central elements needed for understanding of evolutionary processes and phenotypic changes that improve the fitness of populations. It has been hypothesized that rapid adaptive changes in new environments may contribute to the rapid spread and success of invasive plants and animals. As yet, studies of adaptation during invasion are scarce, as is knowledge of the genes underlying adaptation, especially in multiple replicated invasions. Here, we quantified how genotype frequencies change during invasions, resulting in rapid evolution of naturalized populations. We used six fully replicated common garden experiments in Brazil where Pinus taeda (loblolly pine) was introduced at the same time, in the same numbers, from the same seed sources, and has formed naturalized populations expanding outward from the plantations. We used a combination of nonparametric, population genetics and multivariate statistics to detect changes in genotype frequencies along each of the six naturalization gradients and their association with climate as well as shifts in allele frequencies compared to the source populations. Results show 25 genes with significant shifts in genotype frequencies. Six genes had shifts in more than one population. Climate explained 25% of the variation in the groups of genes under selection across all locations, but specific genes under strong selection during invasions did not show climate‐related convergence. In conclusion, we detected rapid evolutionary changes during invasive range expansions, but the particular gene‐level patterns of evolution may be population specific.     

Adaptation to an invasive host is driving the loss of a native ecotype

Locally adapted populations are often used as model systems for the early stages of ecological speciation, but most of these young divergent populations will never become complete species. The maintenance of local adaptation relies on the strength of natural selection overwhelming the homogenizing effects of gene flow; however, this balance may be readily upset in changing environments. Here I show that soapberry bugs (Jadera haematoloma) have lost adaptations to their native host plant (Cardiospermum corindum) and are regionally specializing on an invasive host (Koelreuteria elegans), collapsing a classic and well‐documented example of local adaptation. All populations that were adapted to the native host—including those still found on that host today—are now better adapted to the invasive host in multiple phenotypes. Weak differentiation remains in two traits, suggesting that homogenization across the region is incomplete. This study highlights the potential for adaptation to invasive species to disrupt native communities by swamping adaptation to native conditions through maladaptive gene flow.     

Females of the weevil Zabrotes subfasciatus manipulate the size and number of eggs according to the host seed availability

Abstract. In some insects, the finding of oviposition substrate triggers the uptake into oocytes of yolk proteins that are stored in the fat body during post‐embryonic development. The main host of the bean weevil Zabrotes subfasciatus (Coleoptera; Chrysomelidae; Bruchinae; Amblycerini), in which larval resources are the sole source for future egg maturation, is Phaseolus vulgaris. Despite not feeding as adults, females of this species are able to lay eggs after encountering host seeds but it is not known how females react to changes in the availability of bean seeds. In the present study, the behaviour of Z. subfasciatus facing two very different environments for oviposition is investigated, as well as how this influences offspring fitness. The results obtained show that females of Z. subfasciatus react to variations in the availability of seeds belonging to the same host species by adjusting egg size and number. Females on low bean seed density lay larger and fewer eggs than those on high bean seed density, demonstrating a trade‐off between these reproductive traits. Moreover, females can adjust egg size to changing levels of host availability during the first 4 days of their oviposition period. Although no difference in offspring weight is found, those from small eggs (low competition environment) result in larger adults. No response to selection on these traits after rearing beetles on the same host for 40 generations is observed. This unresponsiveness may indicate that beetle populations behave according to their reaction norm that already allows rapid adaptation to a varying amount of host‐seed availability and better exploitation of the environments of this widespread stored‐seed pest.     

Transcription in space – environmental vs. genetic effects on differential immune gene expression

Understanding how organisms adapt to their local environment is one of the key goals in molecular ecology. Adaptation can be achieved through qualitative changes in the coding sequence and/or quantitative changes in gene expression, where the optimal dosage of a gene's product in a given environment is being selected for. Differences in gene expression among populations inhabiting distinct environments can be suggestive of locally adapted gene regulation and have thus been studied in different species (Whitehead & Crawford 2006 ; Hodgins‐Davis & Townsend 2009 ). However, in contrast to a gene's coding sequence, its expression level at a given point in time may depend on various factors, including the current environment. Although critical for understanding the extent of local adaptation, it is usually difficult to disentangle the heritable differences in gene regulation from environmental effects. In this issue of Molecular Ecology, Stutz et al. ( 2015 ) describe an experiment in which they reciprocally transplanted three‐spined sticklebacks (Gasterosteus aculeatus) between independent pairs of small and large lakes. Their experimental design allows them to attribute differences in gene expression among sticklebacks either to lake of origin or destination lake. Interestingly, they find that translocated sticklebacks show a pattern of gene expression more similar to individuals from the destination lake than to individuals from the lake of origin, suggesting that expression of the targeted genes is more strongly regulated by environmental effects than by genetics. The environmental effect by itself is not entirely surprising; however, the relative extent of it is. Especially when put in the context of local adaptation and population differentiation, as done here, these findings cast a new light onto the heritability of differential gene expression and specifically its relative importance during population divergence and ultimately ecological speciation.     

Embryogenesis plasticity and the transmission of maternal effects in Daphnia pulex

Understanding how genetic, nongenetic, and environmental cues are integrated during development may be critical in understanding if, and how, organisms will respond to rapid environmental change. Normally, only post‐embryonic studies are possible. But in this study, we developed a real‐time, high‐throughput confocal microscope assay that allowed us to link Daphnia embryogenesis to offspring life history variation at the individual level. Our assay identified eight clear developmental phenotypes linked by seven developmental stages, the duration of which were correlated with the expression of specific offspring life history traits. Daphnia embryogenesis varied not only between clones reared in the same environment, but also within a single clone when mothers were of different ages or reared in different food environments. Our results support the hypothesis that Daphnia embryogenesis is plastic and can be altered by changes in maternal state or maternal environment. As well as furthering our understanding of the mechanisms underpinning parental effects, our assay may also have an industrial application if it can be used as a rapid ecotoxicological prescreen for testing the effect that pollutant doses have on offspring life histories traditionally assayed with a 21‐day Daphnia reproduction test.     

Parasite‐mediated selection in a natural metapopulation of Daphnia magna

Parasite‐mediated selection varying across time and space in metapopulations is expected to result in host local adaptation and the maintenance of genetic diversity in disease‐related traits. However, nonadaptive processes like migration and extinction‐(re)colonization dynamics might interfere with adaptive evolution. Understanding how adaptive and nonadaptive processes interact to shape genetic variability in life‐history and disease‐related traits can provide important insights into their evolution in subdivided populations. Here we investigate signatures of spatially fluctuating, parasite‐mediated selection in a natural metapopulation of Daphnia magna. Host genotypes from infected and uninfected populations were genotyped at microsatellite markers, and phenotyped for life‐history and disease traits in common garden experiments. Combining phenotypic and genotypic data a Q_ST–F_ST‐like analysis was conducted to test for signatures of parasite mediated selection. We observed high variation within and among populations for phenotypic traits, but neither an indication of host local adaptation nor a cost of resistance. Infected populations have a higher gene diversity (Hs) than uninfected populations and Hs is strongly positively correlated with fitness. These results suggest a strong parasite effect on reducing population level inbreeding. We discuss how stochastic processes related to frequent extinction‐(re)colonization dynamics as well as host and parasite migration impede the evolution of resistance in the infected populations. We suggest that the genetic and phenotypic patterns of variation are a product of dynamic changes in the host gene pool caused by the interaction of colonization bottlenecks, inbreeding, immigration, hybrid vigor, rare host genotype advantage and parasitism. Our study highlights the effect of the parasite in ameliorating the negative fitness consequences caused by the high drift load in this metapopulation.     

Parallel trait adaptation across opposing thermal environments in experimental Drosophila melanogaster populations

Thermal stress is a pervasive selective agent in natural populations that impacts organismal growth, survival, and reproduction. Drosophila melanogaster exhibits a variety of putatively adaptive phenotypic responses to thermal stress in natural and experimental settings; however, accompanying assessments of fitness are typically lacking. Here, we quantify changes in fitness and known thermal tolerance traits in replicated experimental D. melanogaster populations following more than 40 generations of evolution to either cyclic cold or hot temperatures. By evaluating fitness for both evolved populations alongside a reconstituted starting population, we show that the evolved populations were the best adapted within their respective thermal environments. More strikingly, the evolved populations exhibited increased fitness in both environments and improved resistance to both acute heat and cold stress. This unexpected parallel response appeared to be an adaptation to the rapid temperature changes that drove the cycling thermal regimes, as parallel fitness changes were not observed when tested in a constant thermal environment. Our results add to a small, but growing group of studies that demonstrate the importance of fluctuating temperature changes for thermal adaptation and highlight the need for additional work in this area.     

Secondary invasion of <Emphasis Type="Italic">Acer negundo</Emphasis>: the role of phenotypic responses versus local adaptation

During plant species invasions, the role of adaptive processes is particularly of interest in later stages of range expansion when populations start invading habitats that initially have not been disposed to invasions. The dioecious tree Acer negundo, primarily invasive in Europe in wet habitats along riversides and in floodplains, has increased its abundance in dry habitats of industrial wasteland and ruderal sites during the last decades in Eastern Germany. We chose 21 invasive populations from wet and from dry habitats in the region of Halle, Saxony-Anhalt, Germany, to test whether Acer negundo exhibits a shift in life-history strategy during expansion into more stressful habitats. We analyzed variables of habitat quality (pH, soil moisture, exchangeable cations, total C and N content) and determined density, sex ratio and regeneration of the populations. In addition, we conducted germination experiments and greenhouse studies with seedlings in four different soil moisture environments. Local adaptation was studied in a reciprocal transplant experiment. We found habitat type differentiation with lower nutrient and water supply at the dry sites than at the moist sites and significant differences in the number of seedlings in the field. In accordance, seeds from moist habitats responded significantly faster to germination treatments. In the transplant experiment, leaf life span was significantly larger for populations originating from dry habitat types than from moist habitats. This observed shift in life history strategy during secondary invasion of A. negundo from traits of establishment and rapid growth towards traits connected with persistence might be counteracted by high gene flow among populations of the different habitat types. However, prolonged leaf life span at dry sites contributed remarkably to the invasion of less favourable habitats, and, thus, is a first indication of ongoing adaptation.