Transposable elements in individual genotypes of Drosophila simulans

Transposable elements are abundant, dynamic components of the genome that affect organismal phenotypes and fitness. In Drosophila melanogaster, they have increased in abundance as the species spread out of Africa, and different populations differ in their transposable element content. However, very little is currently known about how transposable elements differ between individual genotypes, and how that relates to the population dynamics of transposable elements overall. The sister species of D. melanogaster, D. simulans, has also recently become cosmopolitan, and panels of inbred genotypes exist from cosmopolitan and African flies. Therefore, we can determine whether the differences in colonizing populations are repeated in D. simulans, what the dynamics of transposable elements are in individual genotypes, and how that compares to wild flies. After estimating copy number in cosmopolitan and African D. simulans, I find that transposable element load is higher in flies from cosmopolitan populations. In addition, transposable element load varies considerably between populations, between genotypes, but not overall between wild and inbred lines. Certain genotypes either contain active transposable elements or are more permissive of transposition and accumulate copies of particular transposable elements. Overall, it is important to quantify genotype‐specific transposable element dynamics as well as population averages to understand the dynamics of transposable element accumulation over time.     

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.     

Transposable DNA elements and life history traits: II. Transposition of P DNA elements in somatic cells reduces fitness, mating activity, and locomotion of Drosophila melanogaster

Some transposable DNA elements in higher organisms are active in somatic cells, as well as in germinal cells. What effect does the movement of DNA elements in somatic cells have on life history traits? It has previously been reported that somatically active P and mariner elements in Drosophila induce genetic damage and significantly reduce lifespan. In this study, we report that the movement of P elements in somatic cells also significantly reduces fitness, mating activity, and locomotion of Drosophila melanogaster. If other elements cause similar changes in life history traits, it is doubtful if transposable DNA elements remain active for long in somatic cells in natural populations.     

The role of the transposable element hobo in the origin of endemic inversions in wild populations of Drosophila melanogaster

Evidence from in situ hybridizations of DNA from the transposable element hobo to polytene salivary gland chromosome squashes reveals that hobo occupies both cytological breakpoints of three of four endemic inversions sampled from natural populations of Drosophila melanogaster in the Hawaiian islands. The fourth endemic inversion has a single hobo insert at one breakpoint. Cosmopolitan inversions on the same chromosomes do not show this association. Frequencies of both endemic and cosmopolitan inversions in Hawaiian populations fall in ranges typical for natural populations of D. melanogaster sampled worldwide, suggesting that these results may be typical of other regions besides Hawaii. This appears to be the first direct demonstration that transposable elements are responsible for causing specific rearrangements found in nature; consequently, it is also the first direct demonstration that chromosome rearrangements can arise in nature in a manner predicted by results of hybrid dysgenic crosses in the laboratory. Possible population genetic and evolutionary consequences are discussed.     

Resistance to oxidative stress shows low heritability and high common environmental variance in a wild bird

Oxidative stress was recently demonstrated to affect several fitness‐related traits and is now well recognized to shape animal life‐history evolution. However, very little is known about how much resistance to oxidative stress is determined by genetic and environmental effects and hence about its potential for evolution, especially in wild populations. In addition, our knowledge of phenotypic sexual dimorphism and cross‐sex genetic correlations in resistance to oxidative stress remains extremely limited despite important evolutionary implications. In free‐living great tits (Parus major), we quantified heritability, common environmental effect, sexual dimorphism and cross‐sex genetic correlation in offspring resistance to oxidative stress by performing a split‐nest cross‐fostering experiment where 155 broods were split, and all siblings (n = 791) translocated and raised in two other nests. Resistance to oxidative stress was measured as both oxidative damage to lipids and erythrocyte resistance to a controlled free‐radical attack. Both measurements of oxidative stress showed low additive genetic variances, high common environmental effects and phenotypic sexual dimorphism with males showing a higher resistance to oxidative stress. Cross‐sex genetic correlations were not different from unity, and we found no substantial heritability in resistance to oxidative stress at adult age measured on 39 individuals that recruited the subsequent year. Our study shows that individual ability to resist to oxidative stress is primarily influenced by the common environment and has a low heritability with a consequent low potential for evolution, at least at an early stage of life.     

X‐AUTOSOME INCOMPATIBILITIES IN DROSOPHILA MELANOGASTER: TESTS OF HALDANE'S RULE AND GEOGRAPHIC PATTERNS WITHIN SPECIES

Substantial genetic variation exists in natural populations of Drosophila melanogaster. This segregating variation includes alleles at different loci that interact to cause lethality or sterility (synthetic incompatibilities). Fitness epistasis in natural populations has important implications for speciation and the rate of adaptive evolution. To assess the prevalence of epistatic fitness interactions, we placed naturally occurring X chromosomes into genetic backgrounds derived from different geographic locations. Considerable amounts of synthetic incompatibilities were observed between X chromosomes and autosomes: greater than 44% of all combinations were either lethal or sterile. Sex‐specific lethality and sterility were also tested to determine whether Haldane's rule holds for within‐species variation. Surprisingly, we observed an excess of female sterility in genotypes that were homozygous, but not heterozygous, for the X chromosome. The recessive nature of these incompatibilities is similar to that predicted for incompatibilities underlying Haldane's rule. Our study also found higher levels of sterility and lethality for genomes that contain chromosomes from different geographical regions. These findings are consistent with the view that genomes are coadapted gene complexes and that geography affects the likelihood of epistatic fitness interactions.     

Parallel effects of the inversion In(3R)Payne on body size across the North American and Australian clines in Drosophila melanogaster

Chromosomal inversions are thought to play a major role in climatic adaptation. In D. melanogaster, the cosmopolitan inversion In(3R)Payne exhibits latitudinal clines on multiple continents. As many fitness traits show similar clines, it is tempting to hypothesize that In(3R)P underlies observed clinal patterns for some of these traits. In support of this idea, previous work in Australian populations has demonstrated that In(3R)P affects body size but not development time or cold resistance. However, similar data from other clines of this inversion are largely lacking; finding parallel effects of In(3R)P across multiple clines would considerably strengthen the case for clinal selection. Here, we have analysed the phenotypic effects of In(3R)P in populations originating from the endpoints of the latitudinal cline along the North American east coast. We measured development time, egg‐to‐adult survival, several size‐related traits (femur and tibia length, wing area and shape), chill coma recovery, oxidative stress resistance and triglyceride content in homokaryon lines carrying In(3R)P or the standard arrangement. Our central finding is that the effects of In(3R)P along the North American cline match those observed in Australia: standard arrangement lines were larger than inverted lines, but the inversion did not influence development time or cold resistance. Similarly, In(3R)P did not affect egg‐to‐adult survival, oxidative stress resistance and lipid content. In(3R)P thus seems to specifically affect size traits in populations from both continents. This parallelism strongly suggests an adaptive pattern, whereby the inversion has captured alleles associated with growth regulation and clinal selection acts on size across both continents.     

IMMUNE RESPONSE TO PARASITISM REDUCES RESISTANCE OF DROSOPHILA MELANOGASTER TO DESICCATION AND STARVATION

Abstract In natural populations, organisms experience simultaneously biotic (e.g., competitors and parasites) and abiotic (e.g., temperature and humidity) stresses. Thus, species must have the capacity to respond to combinations of stressors. How does interaction between biotic and abiotic stress affect organismal performance? To address this question, I studied stress resistance of adult Drosophila melanogaster that survived parasitic attack (as larvae) by the parasitoid Asobara tabida. To determine the impact of genotype on stress resistance, I measured survival under desiccation and starvation of flies within isofemale (genetic) lines. Survivors of parasitism had slightly reduced survivorship compared to unparasitized relatives when both were unstressed, and this difference was exacerbated by desiccation and starvation. These results indicate multiple stressors can compound each other's individual negative effects on fitness. Moreover, isofemale lines differed in their sensitivity to environmental stress and to parasitism. Consequently, genotypic differences in sensitivity to stress may reflect differences in investment priorities between traits that promote survival over other life‐history characters.     

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.     

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.     

Trait‐specific consequences of inbreeding on adaptive phenotypic plasticity

Environmental changes may stress organisms and stimulate an adaptive phenotypic response. Effects of inbreeding often interact with the environment and can decrease fitness of inbred individuals exposed to stress more so than that of outbred individuals. Such an interaction may stem from a reduced ability of inbred individuals to respond plastically to environmental stress; however, this hypothesis has rarely been tested. In this study, we mimicked the genetic constitution of natural inbred populations by rearing replicate Drosophila melanogaster populations for 25 generations at a reduced population size (10 individuals). The replicate inbred populations, as well as control populations reared at a population size of 500, were exposed to a benign developmental temperature and two developmental temperatures at the lower and upper margins of their viable range. Flies developed at the three temperatures were assessed for traits known to vary across temperatures, namely abdominal pigmentation, wing size, and wing shape. We found no significant difference in phenotypic plasticity in pigmentation or in wing size between inbred and control populations, but a significantly higher plasticity in wing shape across temperatures in inbred compared to control populations. Given that the norms of reaction for the noninbred control populations are adaptive, we conclude that a reduced ability to induce an adaptive phenotypic response to temperature changes is not a general consequence of inbreeding and thus not a general explanation of inbreeding–environment interaction effects on fitness components.     

Identification of a candidate adaptive polymorphism for Drosophila life history by parallel independent clines on two continents

Life history traits are critical components of fitness and frequently reflect adaptive responses to environmental pressures. However, few genes that contribute to natural life history variation have been identified. Insulin signalling mediates the determination of life history traits in many organisms, and single gene manipulation in Drosophila melanogaster suggests that individual genes in the pathway have the potential to produce major effects on these quantitative traits. We evaluated allelic variation at two insulin signalling genes, the Insulin‐like Receptor (InR) and its substrate, chico, in natural populations of D. melanogaster. We found different patterns of variation: InR shows evidence of positive selection and clines in allele frequency across latitude; chico exhibits neutral patterns of evolution. The clinal patterns at InR are replicated between North America and Australia, showing striking similarity in the distribution of specific alleles and the rate at which allele frequencies change across latitude. Moreover, we identified a polymorphism at InR that appears to be functionally significant and consistent with hypothetical patterns of selection across geography. This polymorphism provides new characterization of genic regions of functionality within InR, and is likely a component in a suite of genes and traits that respond adaptively to climatic variation.     

Organization and possible origin of the Bari-1 cluster in the heterochromatic h39 region of Drosophila melanogaster

The molecular organization of the heterochromatic h39 region of the Drosophila melanogaster second chromosome has been investigated by studying two BAC clones identified both by Southern blotting and by FISH experiments as containing tandem arrays of Bari1, a transposable element present only in this region. Such BAC clones appear to contain different portions of the h39 region since they differ in the DNA sequences flanking the Bari1 repeats on both sides. Thus, the 80 Bari1 copies estimated to be present in the h39 region are split into at least two separated subregions. On the basis of the analysis of the flanking sequences a possible mechanism depending on an aberrant activity of the Bari1 transposase is proposed for the genesis of the heterochromatic tandem arrays of the element.     

Does Inbreeding and Loss of Genetic Diversity Decrease Disease Resistance?

Inbreeding and loss of genetic diversity are predicted to decrease the resistance of species to disease. However, this issue is controversial and there is limited rigorous scientific evidence available. To test whether inbreeding and loss of genetic diversity affect a host's resistance to disease, Drosophila melanogasterpopulations with different levels of inbreeding and genetic diversity were exposed separately to (a) thuringiensin, an insecticidal toxin produced by some strains of Bacillus thuringiensis, and (b) live Serratia marcescensbacteria. Inbreeding and loss of genetic diversity significantly reduced resistance of D. melanogasterto both the thuringiensin toxin and live Serratia marcescens. For both, the best fitting relationships between resistance and inbreeding were curvilinear. As expected, there was wide variation among replicate inbred populations in disease resistance. Lowered resistances to both the toxin and the pathogen in inbred populations were due to specific resistance alleles, rather than generalized inbreeding effects, as correlations between resistance and population fitness were low or negative. Wildlife managers should strive to minimise inbreeding and loss of genetic diversity within threatened populations and to minimise exposure of inbred populations to disease.     

Competitiveness and life‐history characteristics of Daphnia with respect to susceptibility to a bacterial pathogen

Costs of resistance, i.e. trade‐offs between resistance to parasites or pathogens and other fitness components, may prevent the fixation of resistant genotypes and therefore explain the maintenance of genetic polymorphism for resistance in the wild. Using two approaches, the cost of resistance to a sterilizing bacterial pathogen were tested for in the crustacean Daphnia magna. First, groups of susceptible and resistant hosts from each of four natural populations were compared in terms of their life‐history characteristics. Secondly, we examined the competitiveness of nine clones from one population for which more detailed information on genetic variation for resistance was known. In no case did the results show that competitiveness or life history characteristics of resistant Daphnia systematically differed from susceptible ones. These results suggest that costs of resistance are unlikely to explain the maintenance of genetic variation in D. magna populations. We discuss methods for measuring fitness and speculate on which genetic models of host‐parasite co‐evolution may apply to the Daphnia‐microparasite system.     

Mating success at high temperature in highland‐ and lowland‐derived populations as well as in heat knock‐down selected Drosophila buzzatii

Thermal‐stress selection can affect multiple fitness components including mating success. Reproductive success is one of the most inclusive measures of overall fitness, and mating success is a major component of reproduction. However, almost no attention has been spent to test how mating success can be affected by thermal‐stress selection. In this study, we examine the mating success in the cactophilic Drosophila buzzatii Patterson & Wheeler (Diptera: Drosophilidae) derived from two natural populations that nearly represent the ends of an altitudinal cline for heat knock‐down resistance. Furthermore, we extended the analysis using laboratory lines artificially selected for high and low heat knock‐down resistance. Mating success at high temperature was found to be higher in the lowland than the highland population after a heat pre‐treatment. Moreover, individuals selected for heat knock‐down resistance showed higher mating success at high temperature than did individuals selected for low knock‐down resistance. These results indicate that adaptation to thermal stress can confer an advantage on fitness‐related traits including mating success and highlight the benefits of earlier heat exposure as an adaptive plastic response affecting mating success under stress of higher temperature.     

Themariner transposable element in natural populations ofDrosophila teissieri

Themariner transposable elements of several natural populations ofDrosophila teissieri, a rainforest species endemic to tropical Africa, were studied. Natural populations trapped along a transect from Zimbabwe to the Ivory Coast were analyzed by Southern blotting, in situ hybridization, cloning, and sequencing of PCR products. The Brazzaville population had some full-length elements, while the remaining populations had mainly deleted elements. The main class of deleted elements lacked a 500-bp segment. A mechanism is proposed that could generate such elements rapidly. In situ hybridizations showed that there are nomariner elements in pericentromeric heterochromatin. Finally, the phylogeny of theMos1-likemariner full-length elements is consistent with vertical transmission from the ancestor of themelanogaster subgroup. Correspondence to: P. Capy     

Evolution of total net fitness in thermal lines: Drosophila subobscura likes it 'warm'

Fisher's fundamental theorem states that heritable variation for net fitness sets a limit to the rate of response to natural selection. How will temperate (i.e. cold‐tolerant) species cope with contemporary rapid global warming? Using three‐fold replicated lines of Drosophila subobscura that had been allowed to evolve for 4 years (between 32 and 59 generations) at 13 °C (cold), 18 °C (the supposed optimum temperature), and 22 °C (warm) I assess here how net fitness changes according to thermal environments. Net fitness was estimated following the classical approach in population genetics of competing over a number of generation in outbred experimental populations multiple wild‐type O chromosomes (homologous to arm 3R in D. melanogaster) independently derived from each base thermal stock in an otherwise homogeneous genetic background against a balancer chromosome. Warm‐adapted populations (‘warm‐adapted O chromosomes’) performed comparatively well at all tested temperatures. However, net fitness was severely reduced in cold‐adapted populations when transferred to warmer conditions. It seems, therefore, that thermal fitness breath for D. subobscura flies is positively associated to temperature. These findings are discussed in relation to the fast world‐wide clinal shifts in the frequency of genetic markers correlated with current climate change.