Natural quantitative genetic variance in plant growth differs in response to ecologically relevant temperature heterogeneity

Adaptation to large‐scale spatial heterogeneity in the environment accounts for a major proportion of genetic diversity within species. Theory predicts the erosion of adaptive genetic variation on a within‐population level, but considerable genetic diversity is often found locally. Genetic diversity could be expected to be maintained within populations in temporally or spatially variable conditions if genotypic rank orders vary across contrasting microenvironmental settings. Taking advantage of fine‐resolution environmental data, we tested the hypothesis that temperature heterogeneity among years could be one factor maintaining quantitative genetic diversity within a natural and genetically diverse plant population. We sampled maternal families of Boechera stricta, an Arabidopsis thaliana relative, at one location in the central Rocky Mountains and grew them in three treatments that, based on records from an adjacent weather station, simulated hourly temperature changes at the native site during three summers with differing mean temperatures. Treatment had a significant effect on all traits, with 2–3‐fold increase in above‐ and belowground biomass and the highest allocation to roots observed in the treatment simulating the warmest summer on record at the site. Treatment affected bivariate associations between traits, with the weakest correlation between above‐ and belowground biomass in the warmest treatment. The magnitude of quantitative genetic variation for all traits differed across treatments: Genetic variance of biomass was 0 in the warmest treatment, while highly significant diversity was found in average conditions, resulting in broad‐sense heritability of 0.31. Significant genotype × environment interactions across all treatments were found only in root‐to‐shoot ratio. Therefore, temperature variation among summers appears unlikely to account for the observed levels of local genetic variation in size in this perennial species, but may influence family rank order in growth allocation. Our results indicate that natural environmental fluctuations can have a large impact on the magnitude of within‐population quantitative genetic variance.     

Relationships between spatio-temporal environmental and genetic variation reveal an important influence of exogenous selection in a pupfish hybrid zone

The importance of exogenous selection in a natural hybrid zone between the pupfishes Cyprinodon atrorus and Cyprinodon bifasciatus was tested via spatio‐temporal analyses of environmental and genetic change over winter, spring and summer for three consecutive years. A critical influence of exogenous selection on hybrid zone regulation was demonstrated by a significant relationship between environmental (salinity and temperature) and genetic (three diagnostic nuDNA loci) variation over space and time (seasons) in the Rio Churince system, Cuatro Ciénegas, Mexico. At sites environmentally more similar to parental habitats, the genetic composition of hybrids was stable and similar to the resident parental species, whereas complex admixtures of parental and hybrid genotypic classes characterized intermediate environments, as did the greatest change in allelic and genotypic frequencies across seasons. Within hybrids across the entire Rio Churince system, seasonal changes in allelic and genotypic frequencies were consistent with results from previous reciprocal transplant experiments, which showed C. bifasciatus to suffer high mortality (75%) when exposed to the habitat of C. atrorus in winter (extreme temperature lows and variability) and summer (abrupt salinity change and extreme temperature highs and variability). Although unconfirmed, the distributional limits of C. atrorus and C. atrorus‐like hybrids appear to be governed by similar constraints (predation or competition). The argument favouring evolutionary significance of hybridization in animals is bolstered by the results of this study, which links the importance of exogenous selection in a contemporary hybrid zone between C. atrorus and C. bifasciatus to previous demonstration of the long‐term evolutionary significance of environmental variation and introgression on the phenotypic diversification Cuatro Ciénegas Cyprinodon.     

Overcrowding,food and phosphorus limitation effects on ephipphia production and population dynamics in the invasive species <Emphasis Type="Italic">Daphnia lumholtzi</Emphasis>

Daphnia lumholtzi has been very successful in colonizing North America since its appearance in Texas in 1990. Although previous studies have sought to link its success as an invasive species with various aspects of its population biology, there is little experimental data linking the invasion success of D. lumholtzi with its autecology, specifically its reproduction strategy. In this study we sought to link food quality and quantity to diapause in D. lumholtzi through a variation in phosphorus (P) content of algae, food quantity, and light level. We also assessed the effect of Daphnia peak population densities on reproductive rates and production of resting eggs. We found that when food is abundant, per capita ephippia production may be limited by P, but under food limitation conditions, there is no significant effect of food quality on ephippia production. Our results suggest that a combination of food quality/quantity and population density may work together to induce the production of resting eggs in this invasive species. Handling editor: S. Declerk     

Testing for beneficial reversal of dominance during salinity shifts in the invasive copepod Eurytemora affinis,and implications for the maintenance of genetic variation

Maintenance of genetic variation at loci under selection has profound implications for adaptation under environmental change. In temporally and spatially varying habitats, non‐neutral polymorphism could be maintained by heterozygote advantage across environments (marginal overdominance), which could be greatly increased by beneficial reversal of dominance across conditions. We tested for reversal of dominance and marginal overdominance in salinity tolerance in the saltwater‐to‐freshwater invading copepod Eurytemora affinis. We compared survival of F1 offspring generated by crossing saline and freshwater inbred lines (between‐salinity F1 crosses) relative to within‐salinity F1 crosses, across three salinities. We found evidence for both beneficial reversal of dominance and marginal overdominance in salinity tolerance. In support of reversal of dominance, survival of between‐salinity F1 crosses was not different from that of freshwater F1 crosses under freshwater conditions and saltwater F1 crosses under saltwater conditions. In support of marginal overdominance, between‐salinity F1 crosses exhibited significantly higher survival across salinities relative to both freshwater and saltwater F1 crosses. Our study provides a rare empirical example of complete beneficial reversal of dominance associated with environmental change. This mechanism might be crucial for maintaining genetic variation in salinity tolerance in E. affinis populations, allowing rapid adaptation to salinity changes during habitat invasions.     

A highly pleiotropic amino acid polymorphism in the Drosophila insulin receptor contributes to life‐history adaptation

Finding the specific nucleotides that underlie adaptive variation is a major goal in evolutionary biology, but polygenic traits pose a challenge because the complex genotype–phenotype relationship can obscure the effects of individual alleles. However, natural selection working in large wild populations can shift allele frequencies and indicate functional regions of the genome. Previously, we showed that the two most common alleles of a complex amino acid insertion–deletion polymorphism in the Drosophila insulin receptor show independent, parallel clines in frequency across the North American and Australian continents. Here, we report that the cline is stable over at least a five‐year period and that the polymorphism also demonstrates temporal shifts in allele frequency concurrent with seasonal change. We tested the alleles for effects on levels of insulin signaling, fecundity, development time, body size, stress tolerance, and life span. We find that the alleles are associated with predictable differences in these traits, consistent with patterns of Drosophila life‐history variation across geography that likely reflect adaptation to the heterogeneous climatic environment. These results implicate insulin signaling as a major mediator of life‐history adaptation in Drosophila, and suggest that life‐history trade‐offs can be explained by extensive pleiotropy at a single locus.     

Inducible defences as key adaptations for the successful invasion of Daphnia lumholtzi in North America?

The mechanisms underlying successful biological invasions often remain unclear. In the case of the tropical water flea Daphnia lumholtzi, which invaded North America, it has been suggested that this species possesses a high thermal tolerance, which in the course of global climate change promotes its establishment and rapid spread. However, D. lumholtzi has an additional remarkable feature: it is the only water flea that forms rigid head spines in response to chemicals released in the presence of fishes. These morphologically (phenotypically) plastic traits serve as an inducible defence against these predators. Here, we show in controlled mesocosm experiments that the native North American species Daphnia pulicaria is competitively superior to D. lumholtzi in the absence of predators. However, in the presence of fish predation the invasive species formed its defences and became dominant. This observation of a predator-mediated switch in dominance suggests that the inducible defence against fish predation may represent a key adaptation for the invasion success of D. lumholtzi.     

Predator-induced phenotypic plasticity in the exotic cladoceran Daphnia lumholtzi

1. The exotic cladoceran Daphnia lumholtzi has recently invaded freshwater systems throughout the United States. Daphnia lumholtzi possesses extravagant head spines that are longer than those found on any other North American Daphnia. These spines are effective at reducing predation from many of the predators that are native to newly invaded habitats; however, they are plastic both in nature and in laboratory cultures. The purpose of this experiment was to better understand what environmental cues induce and maintain these effective predator‐deterrent spines. We conducted life‐table experiments on individual D. lumholtzi grown in water conditioned with an invertebrate insect predator, Chaoborus punctipennis, and water conditioned with a vertebrate fish predator, Lepomis macrochirus. 2. Daphnia lumholtzi exhibited morphological plasticity in response to kairomones released by both predators. However, direct exposure to predator kairomones during postembryonic development did not induce long spines in D. lumholtzi. In contrast, neonates produced from individuals exposed to Lepomis kairomones had significantly longer head and tail spines than neonates produced from control and Chaoborus individuals. These results suggest that there may be a maternal, or pre‐embryonic, effect of kairomone exposure on spine development in D. lumholtzi. 3. Independent of these morphological shifts, D. lumholtzi also exhibited plasticity in life history characteristics in response to predator kairomones. For example, D. lumholtzi exhibited delayed reproduction in response to Chaoborus kairomones, and significantly more individuals produced resting eggs, or ephippia, in the presence of Lepomis kairomones.     

Environmental variation alters the fitness effects of rifampicin resistance mutations in Pseudomonas aeruginosa

The fitness effects of antibiotic resistance mutations in antibiotic‐free conditions play a key role in determining the long‐term maintenance of resistance. Although resistance is usually associated with a cost, the impact of environmental variation on the cost of resistance is poorly understood. Here, we test the impact of heterogeneity in temperature and resource availability on the fitness effects of antibiotic resistance using strains of the pathogenic bacterium Pseudomonas aeruginosa carrying clinically important rifampicin resistance mutations. Although the rank order of fitness was generally maintained across environments, fitness effects relative to the wild type differed significantly. Changes in temperature had a profound impact on the fitness effects of resistance, whereas changes in carbon substrate had only a weak impact. This suggests that environmental heterogeneity may influence whether the costs of resistance are likely to be ameliorated by second‐site compensatory mutations or by reversion to wild‐type rpoB. Our results highlight the need to consider environmental heterogeneity and genotype‐by‐environment interactions for fitness in models of resistance evolution.     

Temperature elevation reduces the sensitivity of invasive cladoceran Daphnia lumholtzi to filamentous cyanobacterium Raphidiopsis raciborskii

1. Exotic cladoceran Daphnia lumholtzi is a highly invasive species in the north and south American continents and can potentially also invade European freshwaters and outcompete native Daphnia populations. However, European waterbodies are frequently dominated by less edible filamentous cyanobacteria including also invaders such as Raphidiopsis raciborskii, which might affect the fitness of D. lumholtzi. Furthermore, temperature may influence the sensitivity of D. lumholtzi to R. raciborskii filaments.
2. In this study, we determined whether the presence of R. raciborskii could obstruct the invasion of Europe by D. lumholtzi, through reducing its fitness, and whether this depends on temperature. We compared the population growth rate (r) and the somatic growth rate of D. lumholtzi maintained at two temperatures (20 or 26°C) and fed with two diets: green microalgae alone or green microalgae mixed with filaments of R. raciborskii. Three clones of D. lumholtzi were used to evaluate potential variation in response to the treatments among different clones.
3. At 20°C, the population growth rate of D. lumholtzi fed with cyanobacterial filaments declined sharply. This reduction was caused by increased egg abortion, egg degeneration, and mortality of newborn daphnids. At 26°C, R. raciborskii lost its harmful effect on the population growth of D. lumholtzi. The presence of cyanobacteria did reduce the somatic growth rate of D. lumholtzi at both temperatures and in all three clones except for one that had a similar somatic growth rate on both diets at 26°C.
4. The presence of filamentous cyanobacteria does affect growth in D. lumholtzi and may thereby substantially reduce its invasive potential, but only at lower temperatures. Therefore, the presence of filamentous cyanobacteria may not present an obstacle to the invasion of Europe by D. lumholtzi in a warmer future climate.

     

Leaf morphological plasticity and stomatal conductance in three Populus alba L. genotypes subjected to salt stress

The effect of salt stress on leaf morphology and functionality was studied in three Populus alba genotypes differing in tolerance to salinity: 6K3 (sensitive), 2AS11 (moderately tolerant), and 14P11 (tolerant). Plants were subjected to an intense and progressive salt stress from 50 to 250 mM NaCl by 50 mM steps at 10-day intervals. The micromorphological results highlighted phenotypic variation among the three genotypes already in control plants, with the genotype 14P11 having significantly smaller epidermal cells and higher stomatal density. Salt-treated plants modulated differently the expansion of stomata compared with epidermal cells. Regression analysis showed significant correlations between decrease of stomatal area and stomatal conductance (g_s) in genotypes 14P11 and 6K3. So, the common reduction of stomatal area could be an early mechanism to save water in this species. However, only genotype 14P11 showed further significant decrease of this trait under the highest salinity level, combined with a significant reduction in leaf length. In addition, this genotype showed the lowest leaf abscission rate at the end of salt stress period. The genotype 6K3 was severely affected by leaf necrosis and showed the highest leaf abscission rate in salt stress conditions. In the moderately tolerant genotype 2AS11, an intermediate plastic behaviour in both leaf morphology and physiology was observed during the experiment. The phenotypic variation among the three genotypes in terms of micromorphology and stomatal conductance is discussed in relation to plant functionality in salt stress conditions. Overall results suggest that leaf morphological habit contributes to salt tolerance in P. alba.     

The invasion history of the exotic freshwater zooplankter Daphnia lumholtzi (Cladocera, Crustacea) in North America: a genetic analysis

Daphnia lumholtzi is a planktonic crustacean native to subtropical regions in Africa, Asia and Australia. Since its invasion to the southern USA in ~1990 it has spread across North America as far north as the Laurentian Great Lakes. We assessed invasion history using microsatellite makers and to explore the influence of mean annual temperature on the genetic structure along a latitudinal gradient in North America. Genotypic data were obtained from 9 microsatellite markers for 178 individuals from 13 populations (eight populations introduced to North America and five populations in the native range). Pairwise F_st values as well as Bayesian clustering showed a strong subdivision between native and introduced populations. Bayesian clustering identified multiple genetic clusters in recently invaded locations, suggestive of multiple invasions from various sources, including Asia and Africa. Using variation partitioning, we determined the amount of variation for genetic clusters of populations in the invaded range due to mean annual air temperature and the year of first detection. The results point to a primary introduction into the southern range of North America, with a subsequent northward expansion, and multiple introductions possibly from both the native range and by secondary spread from previously-invaded locations. Separate analysis of genetic clusters within the invaded range suggests additional effects of temperature conditions on geographic genetic structure, possibly as a consequence of D. lumholtzi’s tropical origin.     

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.     

The temporal structure of the environment may influence range expansions during climate warming

Understanding the processes that influence range expansions during climate warming is paramount for predicting population extirpations and preparing for the arrival of non‐native species. While climate warming occurs over a background of variation due to cyclical processes and irregular events, the temporal structure of the thermal environment is largely ignored when forecasting the dynamics of non‐native species. Ecological theory predicts that high levels of temporal autocorrelation in the environment – relatedness between conditions occurring in close temporal proximity – will favor populations that would otherwise have an average negative growth rate by increasing the duration of favorable environmental periods. Here, we invoke such theory to explain the success of biological invasions and evaluate the hypothesis that sustained periods of high environmental temperature can act synergistically with increases in mean temperature to favor the establishment of non‐native species. We conduct a 60‐day field mesocosm experiment to measure the population dynamics of the non‐native cladoceran zooplankter Daphnia lumholtzi and a native congener Daphnia pulex in ambient temperature environments (control), warmed with recurrent periods of high environmental temperatures (uncorrelated‐warmed), or warmed with sustained periods of high environmental temperatures (autocorrelated‐warmed), such that both warmed treatments exhibited the same mean temperature but exhibited different temporal structures of their thermal environments. Maximum D. lumholtzi densities in the warmed‐autocorrelated treatment were threefold and eightfold higher relative to warmed‐uncorrelated and control treatments, respectively. Yet, D. lumholtzi performed poorly across all experimental treatments relative to D. pulex and were undetectable by the end of the experiment. Using mathematical models, we show that this increase in performance can occur alongside increasing temporal autocorrelation and should occur over a broad range of warming scenarios. These results provide both empirical and theoretical evidence that the temporal structure of the environment can influence the performance of species undergoing range expansions due to climate warming.     

Spatiotemporal dynamics and genome‐wide association analysis of desiccation tolerance in Drosophila melanogaster

Water availability is a major environmental challenge to a variety of terrestrial organisms. In insects, desiccation tolerance varies predictably over spatial and temporal scales and is an important physiological determinant of fitness in natural populations. Here, we examine the dynamics of desiccation tolerance in North American populations of Drosophila melanogaster using: (a) natural populations sampled across latitudes and seasons; (b) experimental evolution in field mesocosms over seasonal time; (c) genome‐wide associations to identify SNPs/genes associated with variation for desiccation tolerance; and (d) subsequent analysis of patterns of clinal/seasonal enrichment in existing pooled sequencing data of populations sampled in both North America and Australia. A cline in desiccation tolerance was observed, for which tolerance exhibited a positive association with latitude; tolerance also varied predictably with culture temperature, demonstrating a significant degree of thermal plasticity. Desiccation tolerance evolved rapidly in field mesocosms, although only males showed differences in desiccation tolerance between spring and autumn collections from natural populations. Water loss rates did not vary significantly among latitudinal or seasonal populations; however, changes in metabolic rates during prolonged exposure to dry conditions are consistent with increased tolerance in higher latitude populations. Genome‐wide associations in a panel of inbred lines identified twenty‐five SNPs in twenty‐one loci associated with sex‐averaged desiccation tolerance, but there is no robust signal of spatially varying selection on genes associated with desiccation tolerance. Together, our results suggest that desiccation tolerance is a complex and important fitness component that evolves rapidly and predictably in natural populations.     

Utilization of the exotic cladoceran Daphnia lumholtzi by juvenile fishes in an Illinois River floodplain lake

Daphnia lumholtzi comprises a substantial component of the zooplankton community during mid‐ to late‐summer in Lake Chautauqua, a floodplain lake along the Illinois River near Havana, Illinois. In order to quantify the utilization of D. lumholtzi by juvenile fishes, diet analyses were conducted for seven juvenile fish species collected from Lake Chautauqua during the 2001 annual drawdown period. Freshwater drum Aplodinotus grunniens and emerald shiner Notropis atherinoides demonstrated negative selectivity for D. lumholtzi relative to native zooplankton species whereas four species of fish (bluegill Lepomis macrochirus, white bass Morone chrysops, white crappie Pomoxis annularis and black crappie Pomoxis nigromaculatus) consumed substantial amounts of D. lumholtzi. Although selectivity values for D. lumholtzi varied among these fish species, positive selection for D. lumholtzi increased similarly among larger size classes of each fish species, and corresponded with ontogenetic shifts in diet. Mean body length of D. lumholtzi consumed by 20–69 mm L_T juvenile fishes ranged from 0·75 to 0·99 mm with a calculated total length range of 2·0–2·6 mm. Results from this study provide evidence that high abundances of D. lumholtzi in mid‐ to late‐summer provide an additional food source for several juvenile fish species during a time when abundances of large native cladoceran species (i.e. Daphnia) are low, and juvenile fishes are searching for larger prey associated with ontogenetic shifts from zooplankton to macroinvertebrates and fishes. Because zooplankton production is typically lower in rivers than in lakes, survivorship of juvenile fishes produced in floodplain lakes may be higher in riverine systems if they are not reliant on zooplankton as a primary food resource. Therefore, high abundances of D. lumholtzi may benefit juvenile fishes in managed floodplain lakes, such as Lake Chautauqua, by increasing growth and facilitating the transition from zooplanktivory to insectivory or piscivory.     

Daphnia lumholtzi and Daphnia ambigua: population comparisons of an exotica and a native cladoceran in Lake Okeechobee, Florida

The population dynamics of an exotic cladoceran (Daphnia lumholtzi Sars) and a native cladoceran (Daphnia ambigua) were studied over a 12 month period in subtropical Lake Okeechobee, Florida (USA), to quantify the extent of invasion of the exotic species and compare ecological niches. Daphnia lumholtzi accounted for up to 70% of the Daphnia assemblage during the summer months (June-August), while D.ambigua accounted for up to 97% of the Daphnia assemblage from fall to spring (October-April). The densities of the two species were inversely corelated. The exotic species was most concentrated in the shallower, warmer, north and south ends of the lake during the summer. It also was present, but at much lower densities, in the central lake region during the fall. The native species displayed a ubiquitous distribution throughout the lake during spring and winter, but was concentrated in the deeper, cooler, central region during the summer. Relationships of the two species with environmental conditions indicate that water column temperature might affect the seasonal and spatial distribution of the two Daphnia species. The results also indicate that D.lumholtzi may be filling a 'vacant' seasonal or spatial niche when conditions are unfavorable for D.ambigua.      

Can polyploidy confer invasive plants with a wider climatic tolerance? A test using Solidago canadensis

Polyploidy can cause variation in plant functional traits and thereby generate individuals that can adapt to fluctuating environments and exploit new environments. However, few empirical studies have tested for an association between ploidy level and climatic tolerance of invasive cytotypes relative to conspecific native‐range cytotypes. Here, we used an invasive plant Solidago canadensis to test whether invasive populations had a higher proportion of polyploids, greater height and stem‐base diameter, and occupied a wider range of climatic conditions than conspecific native‐range populations. We also tested whether the invasive populations had overcome genetic founder effects. We sampled a total of 80 populations in parts of the invaded range in China and native range in North America for in situ measurements of plant height and stem‐base diameter in the field and for population genetic and cytotype analyses. To examine climatic correlates, we augmented our field‐sampled data with occurrence records obtained from Global Biodiversity Information Facility. All, except one, of the populations that we sampled in China occurred in a humid subtropical climate. In contrast, the North American populations occurred in humid continental, humid subtropical, and semi‐arid climatic zones. All populations of S. canadensis in China were purely hexaploid, while the North American populations were diploid, tetraploid, and hexaploid. The invasive hexaploids were significantly taller and had a larger stem‐base diameter than native hexaploids. Native hexaploids were significantly taller and had larger stem‐base diameter than native diploids. Climatic correlate assessment found that invasive and native populations occupied different climatic envelopes, with invasive populations occurring in warmer and less seasonal climates than native populations. However, there was no significant correlation between ploidy level and climatic envelope of S. canadensis. Molecular phylogeography data suggest reduced genetic founder effects in the invaded range. Overall, these results suggest that polyploidy does not influence S. canadensis climatic tolerance.