Selection on learning performance results in the correlated evolution of sexual dimorphism in life history

The evolution of learning can be constrained by trade‐offs. As male and female life histories often diverge, the relationship between learning and fitness may differ between the sexes. However, because sexes share much of their genome, intersexual genetic correlations can prevent males and females from reaching their sex‐specific optima resulting in intralocus sexual conflict (IaSC). To investigate if IaSC constraints sex‐specific evolution of learning, we selected Caenorhabditis remanei nematode females for increased or decreased olfactory learning performance and measured learning, life span (in mated and virgin worms), reproduction, and locomotory activity in both sexes. Males from downward‐selected female lines had higher locomotory activity and longer virgin life span but sired fewer progeny than males from upward‐selected female lines. In contrast, we found no effect of selection on female reproduction and downward‐selected females showed higher locomotory activity but lived shorter as virgins than upward‐selected females. Strikingly, selection on learning performance led to the reversal of sexual dimorphism in virgin life span. We thus show sex‐specific trade‐offs between learning, reproduction, and life span. Our results support the hypothesis that selection on learning performance can shape the evolution of sexually dimorphic life histories via sex‐specific genetic correlations.     

Multivariate intralocus sexual conflict in seed beetles

Intralocus sexual conflict (IaSC) is pervasive because males and females experience differences in selection but share much of the same genome. Traits with integrated genetic architecture should be reservoirs of sexually antagonistic genetic variation for fitness, but explorations of multivariate IaSC are scarce. Previously, we showed that upward artificial selection on male life span decreased male fitness but increased female fitness compared with downward selection in the seed beetle Callosobruchus maculatus. Here, we use these selection lines to investigate sex‐specific evolution of four functionally integrated traits (metabolic rate, locomotor activity, body mass, and life span) that collectively define a sexually dimorphic life‐history syndrome in many species. Male‐limited selection for short life span led to correlated evolution in females toward a more male‐like multivariate phenotype. Conversely, males selected for long life span became more female‐like, implying that IaSC results from genetic integration of this suite of traits. However, while life span, metabolism, and body mass showed correlated evolution in the sexes, activity did not evolve in males but, surprisingly, did so in females. This led to sexual monomorphism in locomotor activity in short‐life lines associated with detrimental effects in females. Our results thus support the general tenet that widespread pleiotropy generates IaSC despite sex‐specific genetic architecture.     

Immune priming and pathogen resistance in ant queens

Growing empirical evidence indicates that invertebrates become more resistant to a pathogen following initial exposure to a nonlethal dose; yet the generality, mechanisms, and adaptive value of such immune priming are still under debate. Because life‐history theory predicts that immune priming and large investment in immunity should be more frequent in long‐lived species, we here tested for immune priming and pathogen resistance in ant queens, which have extraordinarily long life span. We exposed virgin and mated queens of Lasius niger and Formica selysi to a low dose of the entomopathogenic fungus Beauveria bassiana, before challenging them with a high dose of the same pathogen. We found evidence for immune priming in naturally mated queens of L. niger. In contrast, we found no sign of priming in virgin queens of L. niger, nor in virgin or experimentally mated queens of F. selysi, which indicates that immune priming in ant queens varies according to mating status and mating conditions or species. In both ant species, mated queens showed higher pathogen resistance than virgin queens, which suggests that mating triggers an up‐regulation of the immune system. Overall, mated ant queens combine high reproductive output, very long life span, and elevated investment in immune defense. Hence, ant queens are able to invest heavily in both reproduction and maintenance, which can be explained by the fact that mature queens will be protected and nourished by their worker offspring.     

Developmental and age-specific effects of selection on divergent virgin life span on fat content and starvation resistance in Drosophila melanogaster

Investigations into the genetic basis of longevity variation have shown life span to be positively correlated with starvation resistance and negatively with female fecundity, both of which rely on lipid content. To assess the firmness of this relation, we assayed correlated responses in age-specific relative fat content (RFC) and starvation resistance in lines successfully selected for divergent virgin life span. We have previously demonstrated that genetic differentiation in female fecundity between our selection lines had disappeared during relaxation of selection. Therefore, we also expected genetic differences in lipid content and starvation resistance to have disappeared. However, RFC and starvation resistance were still significantly lower in short-lived flies than in control flies. Surprisingly, also in long-lived flies RFC and starvation resistance were mostly, but not invariably, found to be significantly lower than in control flies. These results indicate that the genetic correlation of RFC and starvation resistance with reproduction has broken down. Furthermore, the relationship between life span and starvation resistance appears to be more complex than previously anticipated. Also, we could demonstrate that differences in RFC were not brought about by differences in lipid accumulation during adult life, but were already present at eclosion. These findings suggest that pre-adult developmental pathways already impact on the rate of ageing of the adult fly.     

Genetic analysis of extended life span in Drosophila melanogaster I. RAPD screen for genetic divergence between selected and control lines

Using lines selected for long life by Luckinbill and his co-workers, we screened two selected and two control lines for allelic frequency differences at 1200 randomly chosen RAPD marker loci. Twenty-three marker loci showed frequency differences in excess of 80%, and five were greater than 90%. Age-specific effects of the five most differentiated loci were estimated by collecting complete survival data in segregating backcross populations. Alleles at four of the five marker loci were associated with significant extension of life span in males, while two marker loci had significant effects in females. Eighty percent of the total selection response in males can be explained by the identified QTL's, under the assumption of additivity. The N14+ marker allele accounted for a 12-day life span extension in males, but had little effect in females. Both sex-limited and sex-shared effects were observed. Analysis of age-specific mortality rates suggests that life span extension occurs by a combination of genetic factors that moderate both the level of mortality and the rate at which mortality increases with age. This revised version was published online in July 2006 with corrections to the Cover Date.     

Single and multiple mating reduces longevity of female dumpling squid (Euprymna tasmanica)

For many species, mating is a necessary yet costly activity. The costs involved can have an important influence on the evolution of life histories and senescence. Females of many species mate multiply, and this behaviour can inflict a longevity cost. Most studies investigating the effects of multiple mating on female survival have been conducted on insects, and the effects in other taxa are largely unknown. We investigate the effects of both a single mating and a second mating on longevity in female dumpling squid (Euprymna tasmanica), a species in which both sexes mate multiply. Through comparing the longevity of virgin, once‐mated and twice‐mated females, we found that a single mating reduced female life span by 15 days on average. A second mating resulted in an additional 8 day (on average) longevity cost, despite no difference in total clutch mass, number of clutches, single egg mass or number of eggs per clutch between once‐mated and twice‐mated females. This demonstrates a cost to multiple mating which may be independent of the cost of egg production. Furthermore, total clutch mass and female life span were positively correlated, whereas female life span decreased with increasing average water temperature. The presence of an additive effect of reproduction on longevity suggests that multiple mating in cephalopods may have benefits that outweigh these costs, or that there is a conflict in optimal mating frequency between males and females.     

Reduction of mating receptivity and changes in longevity of rice leaf bug, <Emphasis Type="Italic">Trigonotylus caelestialium</Emphasis> (Heteroptera: Miridae), females after mating

To develop new and improved pest management strategies against Trigonotylus caelestialium (Kirkaldy) (Heteroptera: Miridae), a major pest of rice in Japan, it is important to understand the mating behavior of this species. In this study, we examined the effect of mating on subsequent mating receptivity and longevity in female T. caelestialium. After mating, females temporarily exhibited decreased mating receptivity. In addition, the cumulative remating frequency of females that mated with a male that had just mated with another female was higher than that of females who mated with virgin males. As a result, we hypothesized that the male ejaculate reduces female mating receptivity. Furthermore, mated females survived longer without food and water than virgin females; on the other hand, the life span of mated females with access to food and water was less than that for virgin females.     

Quantitative trait locus analysis of male mating success and sperm competition in Drosophila melanogaster

Much of sexual selection theory depends on assumptions about the genetic basis of variation in male mating success and sperm competitive ability. Despite intense interest in this topic, few genes have been identified that contribute to variation in these traits. Here we report the results of quantitative trait locus (QTL) analyses of mating success of male Drosophila melanogaster when exposed to virgin females, remating success of males with previously mated females, and both defense and offense components of sperm competition. We found two to four significant QTLs for remating success, but no QTLs for mating success, even though mating success was more genetically variable than remating success in the recombinant inbred lines used in this study. By combining these results with data from previous gene-expression experiments, we were able to identify three X-linked candidate genes for variation in remating ability. For two of these genes, QTL and expression data were completely concordant with respect to directionality of effects: high mating success was associated with high levels of gene expression and with beneficial QTL effects on the trait. We found equivocal evidence for genetic variation in sperm offense and defense in the recombinant inbred lines, and we did not find any significant QTLs for either sperm competition trait.     

The effect of developmental nutrition on life span and fecundity depends on the adult reproductive environment in Drosophila melanogaster

Both developmental nutrition and adult nutrition affect life‐history traits; however, little is known about whether the effect of developmental nutrition depends on the adult environment experienced. We used the fruit fly to determine whether life‐history traits, particularly life span and fecundity, are affected by developmental nutrition, and whether this depends on the extent to which the adult environment allows females to realize their full reproductive potential. We raised flies on three different developmental food levels containing increasing amounts of yeast and sugar: poor, control, and rich. We found that development on poor or rich larval food resulted in several life‐history phenotypes indicative of suboptimal conditions, including increased developmental time, and, for poor food, decreased adult weight. However, development on poor larval food actually increased adult virgin life span. In addition, we manipulated the reproductive potential of the adult environment by adding yeast or yeast and a male. This manipulation interacted with larval food to determine adult fecundity. Specifically, under two adult conditions, flies raised on poor larval food had higher reproduction at certain ages – when singly mated this occurred early in life and when continuously mated with yeast this occurred during midlife. We show that poor larval food is not necessarily detrimental to key adult life‐history traits, but does exert an adult environment‐dependent effect, especially by affecting virgin life span and altering adult patterns of reproductive investment. Our findings are relevant because (1) they may explain differences between published studies on nutritional effects on life‐history traits; (2) they indicate that optimal nutritional conditions are likely to be different for larvae and adults, potentially reflecting evolutionary history; and (3) they urge for the incorporation of developmental nutritional conditions into the central life‐history concept of resource acquisition and allocation.     

Survival analysis of life span quantitative trait loci in Drosophila melanogaster

We used quantitative trait loci (QTL) mapping to evaluate the age specificity of naturally segregating alleles affecting life span. Estimates of age-specific mortality rates were obtained from observing 51,778 mated males and females from a panel of 144 recombinant inbred lines (RILs). Twenty-five QTL were found, having 80 significant effects on life span and weekly mortality rates. Generation of RILs from heterozygous parents enabled us to contrast effects of QTL alleles with the means of RIL populations. Most of the low-frequency alleles increased mortality, especially at younger ages. Two QTL had negatively correlated effects on mortality at different ages, while the remainder were positively correlated. Chromosomal positions of QTL were roughly concordant with estimates from other mapping populations. Our findings are broadly consistent with a mix of transient deleterious mutations and a few polymorphisms maintained by balancing selection, which together contribute to standing genetic variation in life span.     

ARTIFICIAL SELECTION FOR DEVELOPMENTAL TIME IN DROSOPHILA MELANOGASTER IN RELATION TO THE EVOLUTION OF AGING: DIRECT AND CORRELATED RESPONSES

A wild-type strain of Drosophila melanogaster was successfully selected for both fast and slow larval development. The realized heritabilities (h²) ranged from 0.20 to 0.30 for the fast lines and 0.35 to 0.60 for the slow lines. The selection applied is relevant in relation to the evolution of aging. The longevity of adults, either virgin or mated, was not affected by selection for developmental time, indicating that developmental time is not a causal determinant of life span, thus confirming the results of the studies on environmental effects on aging (Zwaan et al. 1991, 1992). However, adult body weights were higher in the slow developmental lines and lower in the fast lines, relative to the control flies. Furthermore, slow females showed relatively high early fecundity and low late fecundity, as compared with control and fast females. Mated longevities and total lifetime progeny productions were not statistically different. Previous results obtained by other authors from selection experiments on age at reproduction either supported the mutation accumulation or the negative pleiotropy theory of aging (Luckinbill et al. 1984; Rose 1984b). The impact of the reported results on the interpretation of these studies is discussed, and it is noted that direct selection on adult longevity is needed to settle this issue.     

Laboratory evolution of longevity in the bean weevil (Acanthoscelides obtectus)

In this study we examined the effects of long-term selection on early and late reproduction in the bean weevil. The pure lines and the hybrids between the lines within a selection regime were compared for longevity, early and late female fecundity, male mating ability, pre-adult developmental time and wet adult weight. Comparison of hybrid with pure lines provided some evidence for inbreeding despression in the lines from both selection regimes. We found that virgin and mated adults of both sexes from the “old” lines lived longer than “young” line beetles. Comparisons of the hybrid “young” with hybrid “old” lines revealed a trade-off between early and late fecundity of females. For noncompetitive mating ability of males there was no difference between the lines with different rates of senescence when the males were young. But, when the males were older, beetles from the lines selected for delayed senescence expressed superior mating ability. In addition, the “old” line beetles take longer to develop and are heavier than those from “young” line beetles. Although these data suggest that shorter pre-adult developmental time may imply more rapid senescence, there is the possibility of inadvertent selection for rapid development in the “young” lines and this complicates the interpretation of the observed trade-off between the pre-adult and adult performances.     

Reproductive diapause and life-history clines in North American populations of Drosophila melanogaster

Latitudinal clines are widespread in Drosophila melanogaster, and many have been interpreted as adaptive responses to climatic variation. However, the selective mechanisms generating many such patterns remain unresolved, and there is relatively little information regarding how basic life-history components such as fecundity, life span and mortality rates vary across environmental gradients. Here, it is shown that four life-history traits vary predictably with geographic origin of populations sampled along the latitudinal gradient in the eastern United States. Although such patterns are indicative of selection, they cannot distinguish between the direct action of selection on the traits in question or indirect selection by means of underlying genetic correlations. When independent suites of traits covary with geography, it is therefore critical to separate the widespread effects of population source from variation specifically for the traits under investigation. One trait that is associated with variation in life histories and also varies with latitude is the propensity to express reproductive diapause; diapause expression has been hypothesized as a mechanism by which D. melanogaster adults overwinter, and as such may be subject to strong selection in temperate habitats. In this study, recently derived isofemale lines were used to assess the relative contributions of population source and diapause genotype in generating the observed variance for life histories. It is shown that although life span, fecundity and mortality rates varied predictably with geography, diapause genotype explained the majority of the variance for these traits in the sampled populations. Both heat and cold shock resistance were also observed to vary predictably with latitude for the sampled populations. Cold shock tolerance varied between diapause genotypes and the magnitude of this difference varied with geography, whereas heat shock tolerance was affected solely by geographic origin of the populations. These data suggest that a subset of life-history parameters is significantly influenced by the genetic variance for diapause expression in natural populations, and that the observed variance for longevity and fecundity profiles may reflect indirect action of selection on diapause and other correlated traits.     

Simultaneous selection on two fitness-related traits in the butterfly Bicyclus anynana

Abstract. Theory about the role of constraints in evolution is abundant, but few empirical data exist to describe the consequences a bias in phenotypic variation has for micro evolution. Responses to natural selection can be severely hampered by a genetic correlation among a suite of traits. Constraints can be studied using antagonistic selection experiments, that is, two-trait selection in opposition to this correlation. The two traits studied here were development time and wing pattern (eyespot size) in the butterfly Bicyclus anynana , both of which have a clear adaptive significance. Rates of response were higher for eyespot size than for development time, but were independent of the concurrent selection (either in the same direction as the correlation or perpendicular to it). Regimes differed in both traits in all directions after 11 generations of selection. The uncoupling lines had higher relative responses than the synergistic lines in development time and equal relative responses in eyespot size. The patterns for eyespot size (reaction norms) were consistent across different rearing temperatures. Differences in lines selected for fast and slow development time were more pronounced at lower temperatures, irrespective of the direction of joint wing pattern selection. Furthermore, correlated responses in pupal weight and growth rate were observed; lines selected for a slower development had higher pupal weights, especially at lower temperatures. The response of the uncoupling lines was not hampered by a lack of selectable genetic variation, and the relative response in the development time was larger than expected based on response in the coupled direction and quantitative genetic predictions. This suggests that the structure of the genetic architecture does not constrain the short-term, independent evolution of both wing pattern and development time.     

Direct and correlated responses to artificial selection on male mating frequency in the stalk-eyed fly Cyrtodiopsis dalmanni

Traditionally it was thought that fitness-related traits such as male mating frequency, with a history of strong directional selection, should have little additive genetic variance and thus respond asymmetrically to bidirectional artificial selection. However, recent findings and theory suggest that a balance between selection for increased male mating frequency and opposing selection pressures on physiologically linked traits will cause male mating frequency to have high additive genetic variation and hence respond symmetrically to selection. We tested these hypotheses in the stalk-eyed fly, Cyrtodiopsis dalmanni, in which males hold harems comprising many females and so have the opportunity to mate at extremely high frequencies. We subjected male stalk-eyed flies to artificial selection for increased ('high') and decreased ('low') mating frequency in the presence of ecologically realistic, high numbers of females. High line males mated significantly more often than control or low line males. The direct response to selection was approximately symmetric in the high and low lines, revealing high additive genetic variation for, and no significant genetic constraints on, increased male mating frequency in C. dalmanni. In order to investigate trade-offs that might constrain male mating frequency under natural conditions we examined correlated responses to artificial selection. We measured accessory gland length, testis length and eyespan after 7 and 14 generations of selection. High line males had significantly larger accessory glands than low line males. No consistent correlated responses to selection were found in testis length or eyespan. Our results suggest that costs associated with the production and maintenance of large accessory glands, although yet to be identified, are likely to be a major constraint on mating frequency in natural populations of C. dalmanni.     

Genetic analysis of extended life span in Drosophila melanogaster II. Replication of the backcross test and molecular characterization of the N14 Locus

We are interested in localizing chromosomal regions that extend life span in Drosophila. Using stocks artificially selected for long life by Luckinbill and his colleagues, we have identified marker loci that are highly divergent in allelic frequencies between replicated long-lived lines and controls (Curtsinger et al., 1998). Several of the most divergent loci have been found to be associated with effects on life span in segregating backcross populations. Here we report an independent replication of the backcross test for the N14 marker locus, previously reported to extend male life spans by 12 days. The life span effect successfully replicates in males. N14 accounts for 30% of the total selection response in males. Life span extension occurs by a decrease in age-specific mortality rates at all ages, and is not attributable to modification of the slope of the age-specific mortality curve. The effect in females is small or nonexistent. Sequencing of the N14 locus shows that it is non-coding and not obviously regulatory, suggesting that the phenotypic effect arises from linkage disequilibrium with another locus or loci that directly affect life span. N14 DNA hybridizes to 63F/64A on the left arm of chromosome 3. The location is consistent with previous whole-chromosome substitution studies, and suggests new candidate genes for life span extension in Drosophila, including ras2. This revised version was published online in July 2006 with corrections to the Cover Date.     

Behavior of triatomines (Hemiptera:Reduviidae) vectors of Chagas' disease. IV. Fecundity, fertility and longevity of Panstrongylus megistus (Burm., 1835) pairs and virgin females starved under laboratory conditions

A laboratory study was conducted on the fecundity, fertility and life span of Panstrongylus megistus pairs and on the fecundity and life span of P. megistus virgin females submitted to starvation after the last moulting. Of the mated females, 22.2% laid eggs, 4.4% of which were fertile. Females resisted starvation more than males. Of the starved virgin females, only 10% laid eggs, with a low egg-laying rate (0.47) per female. Resistance to starvation was lower in virgin than in mated females.     

Adaptive diversity in genetic control of egg-laying behavior in Drosophila melanogaster

Summary

In the absence of insemination or of a suitable oviposition site, Drosophila melanogaster females react with egg retention patterns which differ as to the position in the genital tract at which the mechanism operates (ovarioles for initial retention; uterus for oviposition blocking) and to physiological basis. A study of the first laboratory generation of isofemale lines, founded by using three different samples of wild flies collected the same year from a natural population, showed a significant genetic variability in initial egg retention by virgin females and in the capacity for oviposition blocking by mated flies reacting to an unfavorable oviposition site. Comparison of isofemale lines showed that these two adaptive behavior patterns also differ in their genetic determination. They are controlled, and therefore can react, independently to selection pressures resulting from seasonal variation in the natural environment.     

GENETIC,ACCLIMATIZATION, AND ONTOGENETIC EFFECTS ON HABITAT SELECTION BEHAVIOR IN DAPHNIA PULICARIA

Daphnia pulicaria from three different populations were observed to express within-population variation in habitat-choice behavior in field assays. Individuals from different habitats (i.e., lake depths) were isolated and cultured as clonal lines under standard conditions. Habitat choices by clonal descendants were then estimated in the field, using replicate experimental columns. There was significant heritable and ontogenetic variation in habitat choice, but the heritable effect was small relative to the phenotypic variation of the original isolates. In a second set of experiments, D. pulicaria that were acclimatized to different habitats showed a strong tendency to choose the habitat to which they had been acclimatized. These data suggest that a given genotype can use a wide range of habitats, given appropriate acclimatization. Although genetic variation is significant, we hypothesize that natural selection on correlated ecological traits is more likely to maintain patterns of genotypic segregation among habitats in Daphnia.     

Estimates of genetic parameters of certain characters in Hevea brasiliensis

Summary Heritability estimates of five quantitative characters, namely, yield, girth, girth increment, virgin bark and renewed bark thickness, of the breeding Phase III Hevea families have been obtained by variance component analyses. In general, the combined heritability estimates for various characters were low to moderate. The heritabilities of these characters based on female variance components, however, were high, suggesting that considerable improvement of each of the characters could be achieved in properly designed experiments.Estimates of heritability for average yields (Range: 0.11–0.34) over different years showed that the first three years' yield was adequate for predicting estimates of genetic variance for the average of five years' yield.Correlation studies on yield with other characters indicated considerable influence of environment, with genetic correlations accounting for about 0.07 to 0.36 in the characters studied.Expected direct response to selection in yield and correlated response in yield to selection for girth at opening and virgin bark thickness have been calculated using three arbitrary values of selection intensity. The efficiency of the correlated response was found to be approximately half that of the direct response. However, the indirect selection for yield using virgin bark thickness appeared to be more favourable than that using the girth at opening favoured by earlier workers.