ALTERNATIVE ROUTES TO THE EVOLUTION OF COMPETITIVE ABILITY IN TWO COMPETING SPECIES OF DROSOPHILA

The evolution of components of interspecific competitive ability was examined in three different environments for three replicate pairs of Drosophila melanogaster and D. simulans populations. Populations evolved enhanced competitive ability in three ways: (1) increased effectiveness at reducing the numbers of the competitor species; (2) increased resistance to the inhibitory effects of the competitor species; or (3) a combination of the two. Considerable variation was seen in the evolutionary outcomes of competition among environments, and also among replicate populations within environments. Significant replicate-by-environment interactions were also observed. The results suggest that the evolutionary routes to the evolution of enhanced competitive abilities can potentially differ among subdivided populations, creating a geographic mosaic of outcomes.     

INTERSPECIFIC LABORATORY COMPETITION OF THE RECENTLY SYMPATRIC SPECIES DROSOPHILA SUBOBSCURA AND DROSOPHILA PSEUDOOBSCURA

Abstract.—Drosophila subobscura and D. pseudoobscura are closely related species coexisting on the West Coast of North America, which was recently colonized by D. subobscura. In competition experiments with overlapping generations, D. subobscura is eliminated by D. pseudoobscura in a few generations at all four temperatures and two initial frequencies tested. Yet in one-species cultures, D. subobscura thrives at all experimental conditions. Single-generation competition experiments reveal lower survivorship and productivity of D. subobscura at all temperatures and frequencies. Productivity per female is dependent on the initial frequencies: greater for D. subobscura as its initial frequency becomes higher, but lower for D. pseudoobscura as its frequency becomes higher. Strains of D. subobscura from three disparate geographic origins yield similar results.     

SPERM COMPETITIVE ABILITY AND INDICES OF LIFETIME REPRODUCTIVE SUCCESS

Understanding the selection pressures shaping components of male reproductive success is essential for assessing the role of sexual selection on phenotypic evolution. A male's competitive reproductive success is often measured in sequential mating tests by recording P1 (first mating male) and P2 (second mating male) paternity scores. How each of these scores relates to a male's overall fitness, for example, lifetime reproductive success is, however, not known. This information is needed to determine whether males benefit from maximizing both P1 and P2 or by trading off P1 against P2 ability. We measured P1, P2, and an index of lifetime reproductive success (LRS_i, a male's competitive reproductive success measured over 12 days) for individual male Drosophila melanogaster. We found no evidence for phenotypic correlations between P1 and P2. In addition, whereas both P1 and P2 were associated with relative LRS_i, only P2 predicted absolute LRS_i. The results suggest that P2 was most closely linked to LRS_i in the wild‐type population studied, a finding which may be common to species with strong second male sperm precedence. The study illustrates how P1 and P2 can have differing relationships with a male's overall reproductive success, and highlights the importance of understanding commonly used measures of sperm competition in the currency of fitness.     

断根对冬小麦竞争能力与产量的影响

 采用简化的deWit替代系列法研究了盆栽冬小麦‘长武135’（Triticum aestivum cv. Changwu 135）在拔节初期断根对冬小麦根冠关系、竞争能力及其与产量性状的关系。无论干旱或湿润，单栽条件下断根降低了小麦的根冠比，在混栽条件下，断根小麦的相对穗重和相对地上部生物量均显著低于未断根小麦，说明断根降低了小麦的竞争能力。根冠比越大竞争能力越强，即作物的竞争能力与根冠比存在正相关关系。单栽湿润条件,断根降低了小麦的穗重和籽粒产量，而在中等干旱条件下，断根小麦穗重和籽粒产量高于未断根小麦 。说明在水资源充分的条件下，较高的作物个体竞争能力则具有较高的生产能力，而在水资源有限的情况下，降低作物个体竞争能力反而提高了群体籽粒产量。     

LABORATORY EVOLUTION OF LONGEVITY AND REPRODUCTIVE FITNESS COMPONENTS IN MALE FRUIT FLIES: MATING ABILITY

Populations of Drosophila melanogaster that had been selected for divergent rates of senescence were compared with respect to age-specific male mating ability. The competitive mating ability of males from populations with delayed senescence was inferior to that of males from populations with higher rates of senescence when males were young. This relationship was reversed when males were older. For noncompetitive mating ability and for recovery of fertility after an exhaustive mating bout, there was no difference between populations with different rates of senescence when males were young. However when males were older, flies from populations selected for delayed senescence again had superior mating ability. Thus, rates of male reproductive senescence can be altered in predictable ways by natural selection. The results for the competitive mating tests are consistent with the hypothesis that antagonistic gene action between early- and late-life fitness components influences the evolution of senescence in these populations.     

FLUCTUATING TEMPERATURE LEADS TO EVOLUTION OF THERMAL GENERALISM AND PREADAPTATION TO NOVEL ENVIRONMENTS

Environmental fluctuations can select for generalism, which is also hypothesized to increase organisms’ ability to invade novel environments. Here, we show that across a range of temperatures, opportunistic bacterial pathogen Serratia marcescens that evolved in fluctuating temperature (daily variation between 24°C and 38°C, mean 31°C) outperforms the strains that evolved in constant temperature (31°C). The growth advantage was also evident in novel environments in the presence of parasitic viruses and predatory protozoans, but less clear in the presence of stressful chemicals. Adaptation to fluctuating temperature also led to reduced virulence in Drosophila melanogaster host, which suggests that generalism can still be costly in terms of reduced fitness in other ecological contexts. While supporting the hypothesis that evolution of generalism is coupled with tolerance to several novel environments, our results also suggest that thermal fluctuations driven by the climate change could affect both species’ invasiveness and virulence.     

SEX AND SPECIATION: GENETIC ARCHITECTURE AND EVOLUTIONARY POTENTIAL OF SEXUAL VERSUS NONSEXUAL TRAITS IN THE SIBLING SPECIES OF THE DROSOPHILA MELANOGASTER COMPLEX

Phenotypic divergence in the male reproductive system (genitalia and gonads) between species of the Drosophila melanogaster complex and their hybrids was quantified to decipher the role of these traits in species differentiation and speciation. Internal as well as external, sexual and nonsexual traits were analyzed with respect to genetic variation and trait asymmetry between strains within species, genetic divergence between species, and dominance and asymmetry in species and hybrids. The variation between strains within species was significant among sexual traits, and only external traits were less asymmetric than internal ones, which suggests that sexual traits are not strongly constrained within species. Three main findings show that sexual traits are most divergent between species: (1) testis length and area, and the area of the posterior lobe of the genital arch (sexual traits) showed the highest proportion of variation between species; (2) linear discriminant functions with the highest components associated to sexual traits were better predictors of species membership; and (3) testis length and area revealed a departure from a linear relationship between members of the species group. Examination of interspecific hybrids showed that sexual traits had higher asymmetry in species hybrids than in the parental species and that sexual traits showed additivity or dominance whereas nonsexual traits showed overdominance (with the exception of malpighian tubules length). These results suggest that sexual traits have undergone more genetic changes and, as a result, tend to show higher divergence and stronger hybrid breakdown between species than nonsexual traits. We propose that sexual selection in the broad sense, affecting all aspects of sexuality, may be responsible for the diversified appearance of sexual traits among closely related species and that the genetic architecture underlying sexual traits may be more prone to disruption during the early stages of speciation.     

EXPERIMENTAL EVOLUTION OF HSP70 EXPRESSION AND THERMOTOLERANCE IN DROSOPHILA MELANOGASTER

To examine whether recent evolutionary history affects the expression of Hsp70, the major heat-induced-heat shock protein in Drosophila melanogaster, we measured Hsp70 expression, thermotolerance, and hsp70 gene number in replicate populations undergoing laboratory evolution at different temperatures. Despite Hsp70's ancient and highly conserved nature, experimental evolution effectively and replicably modified its expression and phenotype (thermotolerance). Among five D. melanogaster populations founded from a common ancestral population and raised at three different temperatures (one at 18°C, two each at 25°C and 28°C) for twenty years, Hsp70 expression varies in a consistent pattern: the replicate 28°C lines expressed 30–50% less Hsp70 than the other lines at a range of inducing temperatures. This modification was refractory to acclimation, and correlated with thermotolerance: the 28°C lines had significantly lower inducible tolerance of 38.5°C and 39°C. We verified the presence of five hsp70 genes in the genome of each line, excluding copy number variation as a candidate molecular basis of the evolved difference in expression. These findings support the ability of Hsp70 levels in D. melanogaster populations to change over microevolutionary time scales and implicate constancy of environmental temperature as a potentially important selective agent.     

EVOLUTION AND DEVELOPMENT OF BODY SIZE AND CELL SIZE IN DROSOPHILA MELANOGASTER IN RESPONSE TO TEMPERATURE

We examined the evolutionary and developmental responses of body size to temperature in Drosophila melanogaster, using replicated lines of flies that had been allowed to evolve for 5 yr at 25°C or at 16.5°C. Development and evolution at the lower temperature both resulted in higher thorax length and wing area. The evolutionary effect of temperature on wing area was entirely a consequence of an increase in cell area. The developmental response was mainly attributable to an increase in cell area, with a small effect on cell number in males. Given its similarity to the evolutionary response, the increase in body size and cell size resulting from development at low temperature may be a case of adaptive phenotypic plasticity. The pattern of plasticity did not evolve in response to temperature for any of the traits. The selective advantage of the evolutionary and developmental responses to temperature is obscure and remains a major challenge for future work.     

EVOLUTION OF DRIVING X CHROMOSOMES AND RESISTANCE FACTORS IN EXPERIMENTAL POPULATIONS OF DROSOPHILA SIMULANS

Sex-ratio drive is a particular case of meiotic drive, described in several Drosophila species, that causes males bearing driving X chromosome to produce a large excess of females in their progeny. In Drosophila simulans, driving X chromosomes and resistance factors located on the Y chromosome and on the autosomes have been previously reported. In this paper, we report the study of the dynamics of sex-ratio factors in experimental populations. We followed the evolution in frequency of driving X chromosomes in the absence of resistance factors and the evolution of resistance factors in the presence of driving X chromosomes. The driving X chromosome was lost, contrarily to theoretical expectations that predict its rapid invasion. Autosomal resistances increased in frequency, and resistant Y chromosomes invaded the population very quickly, as predicted by theoretical models. Fitness measurements showed that the loss of the driving X chromosome was due to a strong deleterious effect that was expressed only when distorting males were in competition with standard males. However, the spread of autosomal resistances reduced this deleterious effect. Implications for the maintenance of polymorphism in natural populations are discussed.     

COMPLEX TRADE-OFFS AND THE EVOLUTION OF STARVATION RESISTANCE IN DROSOPHILA MELANOGASTER

The measurement of trade-offs may be complicated when selection exploits multiple avenues of adaptation or multiple life-cycle stages. We surveyed 10 populations of Drosophila melanogaster selected for increased resistance to starvation for 60 generations, their paired controls, and their mutual ancestors (a total of 30 outbred populations) for evidence of physiological and life-history trade-offs that span life-cycle stages. The directly selected lines showed an impressive response to starvation selection, with mature adult females resisting starvation death 4–6 times longer than unselected controls or ancestors—up to a maximum of almost 20 days. Starvation-selected flies are already 80% more resistant to starvation death than their controls immediately upon eclosion, suggesting that a significant portion of their selection response was owing to preadult growth and acquisition of metabolites relevant to the stress. These same lines exhibited significantly longer development and lower viability in the larval and pupal stages. Weight and lipid measurements on one of the starvation-selected treatments (SB_1–5), its control populations (CB_1–5), and their ancestor populations (B_1–5) revealed three important findings. First, starvation resistance and lipid content were linearly correlated; second, larval lipid acquisition played a major role in the evolution of adult starvation resistance; finally, increased larval growth rate and lipid acquisition had a fitness cost exacted in reduced viability and slower development. This study implicates multiple life-cycle stages in the response to selection for the stress resistance of only one stage. Our starvation-selected populations illustrate a case that may be common in nature. Patterns of genetic correlation may prove misleading unless multiple pleiotropic interconnections are resolved.     

RESOURCE ACQUISITION AND THE EVOLUTION OF STRESS RESISTANCE IN DROSOPHILA MELANOGASTER

Resistance to environmental stress is one of the most important forces molding the distribution and abundance of species. We investigated the evolution of desiccation stress resistance using 20 outbred Drosophila melanogaster populations directly selected in the laboratory for adult desiccation resistance (D), postponed senescence (O), and their respective controls (C and B). Both aging and desiccation selection increased desiccation resistance relative to their controls, creating a spectrum of desiccation resistance levels across selection treatments. We employed an integrative approach, merging data on the life histories of these populations with a detailed physiology of water balance. The physiological basis of desiccation resistance may be mechanisms enhancing either resource conservation or resource acquisition and allocation. Desiccation-resistant populations had increased water and carbohydrate stores, and showed age-specific patterns of desiccation resistance consistent with the resource accumulation mechanism. A significant proportion of the resources relevant to resistance of the stress were accumulated in the larval stage. Males and females of desiccation-selected lines exhibited distinctly different patterns of desiccation resistance and resource acquisition, in a manner suggesting intersexual antagonism in the evolution of stress resistance. Preadult viability of stress-selected populations was lower than that of controls, and development was slowed. Our results suggest that there is a cost to preadult resource acquisition, pointing out a complex trade-off architecture involving characters distributed across distinct life-cycle stages.     

ADAPTATION AND SPECIALIZATION IN A TWO-RESOURCE ENVIRONMENT IN DROSOPHILA SPECIES

We assayed two components of performance (development time and survivorship), on food medium with and without ethanol, in laboratory populations of Drosophila simulans and D. melanogaster for which ethanol-medium was a novel food resource. These assays were done before and after 12 generations of rearing in either one-(regular medium only) or two-resource (regular medium and ethanol medium) environments. Initially, D. simulans was highly susceptible to ethanol, whereas D. melanogaster was relatively unaffected. After 12 generations in the two-resource environment, D. simulans showed significantly improved mean performance on ethanol medium; mean performance of D. melanogaster did not significantly change. Variation among families for both traits was higher on ethanol medium in D. simulans. Variation in D. melanogaster was not significantly affected by ethanol level, suggesting that resource quality was more important than novelty per se. In both species, the least variation was seen in populations after 12 generations in the two-resource environment. For development time in D. simulans, the decrease in variation was largely due to reduced variation within families, suggesting the evolution of canalization. Development time on the two media was not negatively correlated. In D. simulans, correlations measured before and after the experiment were not heterogeneous, suggesting that trade-offs in performance did not block diet expansion. In D. melanogaster, correlations became significantly less positive after 12 generations in the two-resource environment, supporting the view that correlations between performance on different resources may become less positive over time through selection.     

ON THE EVOLUTION OF MIGRATION IN HETEROGENEOUS ENVIRONMENTS

Populations often experience variable conditions, both in time and space. Here we develop a novel theoretical framework to study the evolution of migration under the influence of spatially and temporally variable selection and genetic drift. First, we examine when polymorphism is maintained at a locus under heterogeneous selection, as a function of the pattern of spatial heterogeneity and the migration rate. In a second step, we study how levels of migration evolve under the joint action of kin competition and local adaptation at a polymorphic locus. This analysis reveals the existence of evolutionary bistability, whereby a low or a high migration rate may evolve depending on the initial conditions. Last, we relax several assumptions regarding selection heterogeneity commonly made in previous studies and explore the consequences of more complex spatial and temporal patterns of variability in selection on the evolution of migration. We found that small modifications in the pattern of environmental heterogeneity may have dramatic effects on the evolution of migration. This work highlights the importance of considering more general scenarios of environmental heterogeneity when studying the evolution of life‐history traits in ecologically complex settings.     

THE INFLUENCE OF ABDOMINAL PIGMENTATION ON DESICCATION AND ULTRAVIOLET RESISTANCE IN TWO SPECIES OF DROSOPHILA

Drosophila yakuba and D. santomea are sister species that differ in their levels of abdominal pigmentation; D. yakuba shows heavily pigmented posterior abdominal segments in both sexes, whereas D. santomea lacks dark pigment anywhere on its body. Using naturally collected lines, we demonstrate the existence of altitudinal variation in abdominal pigmentation in D. yakuba but not in D. santomea. We use the variation in pigmentation within D. yakuba and two body‐color mutants in D. yakuba to elucidate selective advantage of differences in pigmentation. Our results indicate that although differences in abdominal pigmentation have no effect on desiccation resistance, lighter pigmentation confers ultraviolet radiation resistance in this pair of species.     

GENETICS OF SEXUAL ISOLATION AND COURTSHIP DYSFUNCTION IN MALE HYBRIDS OF DROSOPHILA PSEUDOOBSCURA AND DROSOPHILA PERSIMILIS

Despite the importance of sexual isolation to speciation, few studies have analyzed the genetic basis of interspecific mating discrimination, particularly using hybrid males. In this study, I investigated the genetic basis of sexual isolation using male hybrids of Drosophila pseudoobscura and D. persimilis. Hybrid male mating success was caused by interactions between the X-chromosome and autosomes (or Y-chromosome), and different arms of the X-chromosome contributed to mating success with females of each species. Further, although there was an X-chromosome component to mating success, its magnitude was not disproportionately large when compared with the proportion of the genome contained on this chromosome. Some hybrid males courted with an anomalously low intensity, so I simultaneously mapped the genetic basis of this “courtship dysfunction.” The courtship dysfunction was caused by an interaction between the left arm of the X-chromosome in D. persimilis with the autosomes or Y-chromosome from D. pseudoobscura. Anomalous courtship behavior in interspecific hybrids can obscure the conclusions of studies of the genetics of sexual isolation, so courtship intensity should be evaluated in all such investigations.     

EVOLUTION OF STARVATION RESISTANCE IN DROSOPHILA MELANOGASTER: ASPECTS OF METABOLISM AND COUNTER-IMPACT SELECTION

An artificial selection experiment for increased female starvation resistance employed five selected lines and five control lines of Drosophila melanogaster. Females responded to selection within the first five generations, but a substantial male response was not observed until starvation resistance was assessed at generation 15. By measuring respiration rate in selected and control lines, it was possible to test the hypothesis that reduced metabolic rate is a general mechanism for stress resistance. There was no association between starvation resistance and respiration rate and thus no support for the hypothesis. Studies using vertebrates have shown that starvation causes a decrease in intermediary metabolism enzyme activity, but this relationship is not well documented in invertebrates. In the present study, intermediary metabolism enzyme activities decreased in response to starvation in control-line females and males, and in selected-line males. However, the selected females showed no overall decrease in enzyme activities in response to starvation. One interpretation is that selected females evolved to resist the phenotypic impact of stress. The concept of “counter-impact selection” is discussed in relationship to the use of phenotypic manipulations for the study of evolution.     

WOLBACHIA AND THE EVOLUTION OF REPRODUCTIVE ISOLATION BETWEEN DROSOPHILA RECENS AND DROSOPHILA SUBQUINARIA

Endosymbiotic bacteria of the genus Wolbachia are widespread among insects and in many cases cause cytoplasmic incompatibility in crosses between infected males and uninfected females. Such findings have been used to argue that Wolbachia have played an important role in insect speciation. Theoretical models, however, indicate that Wolbachia alone are unlikely to lead to stable reproductive isolation between two formerly conspecific populations. Here we analyze the components of reproductive isolation between Drosophila recens, which is infected with Wolbachia, and its uninfected sister species Drosophila subquinaria. Laboratory pairings demonstrated that gene flow via matings between D. recens females and D. subquinaria males is hindered by behavioral isolation. Matings readily occurred in the reciprocal cross (D. quinaria females × D. recens males), but very few viable progeny were produced. The production of viable hybrids via this route was restored by antibiotic curing of D. recens of their Wolbachia symbionts, indicating that hybrid offspring production is greatly reduced by cytoplasmic incompatibility in the crosses involving infected D. recens males. Thus, behavioral isolation and Wolbachia-induced cytoplasmic incompatibility act as complementary asymmetrical isolating mechanisms between these two species. In accordance with Haldane's rule, hybrid females were fertile, whereas hybrid males invariably were sterile. Levels of mtDNA variation in D. recens are much lower than in either D. subquinaria or D. falleni, neither of which is infected with Wolbachia. The low haplotype diversity in D. recens is likely due to an mtDNA sweep associated with the spread of Wolbachia. Nevertheless, the existence of several mtDNA haplotypes in this species indicates that Wolbachia have been present as a potential isolating mechanism for a substantial period of evolutionary time. Finally, we argue that although Wolbachia by themselves are unlikely to bring about speciation, they can increase the rate of speciation in insects.     

DENSITY-DEPENDENT NATURAL SELECTION IN DROSOPHILA: EVOLUTION OF GROWTH RATE AND BODY SIZE

Drosophila melanogaster populations subjected to extreme larval crowding (CU lines) in our laboratory have evolved higher larval feeding rates than their corresponding controls (UU lines). It has been suggested that this genetically based behavior may involve an energetic cost, which precludes natural selection in a density-regulated population to simultaneously maximize food acquisition and food conversion into biomass. If true, this stands against some basic predictions of the general theory of density-dependent natural selection. Here we investigate the evolutionary consequences of density-dependent natural selection on growth rate and body size in D. melanogaster. The CU populations showed a higher growth rate during the postcritical period of larval life than UU populations, but the sustained differences in weight did not translate into the adult stage. The simplest explanation for these findings (that natural selection in a crowded larval environment favors a faster food acquisition for the individual to attain the same final body size in a shorter period of time) was tested and rejected by looking at the larva-to-adult development times. Larvae of CU populations starved for different periods of time develop into comparatively smaller adults, suggesting that food seeking behavior in a food depleted environment carries a higher cost to these larvae than to their UU counterparts. The results have important implications for understanding the evolution of body size in natural populations of Drosophila, and stand against some widespread beliefs that body size may represent a compromise between the conflicting effects of genetic variation in larval and adult performance.