Humidity affects genetic architecture of heat resistance in Drosophila melanogaster

Laboratory experiments on Drosophila have often demonstrated increased heritability for morphological and life‐history traits under environmental stress. We used parent–offspring comparisons to examine the impact of humidity levels on the heritability of a physiological trait, resistance to heat, measured as knockdown time at constant temperature. Drosophila melanogaster were reared under standard nonstressful conditions and heat‐shocked as adults at extreme high or low humidity. Mean knockdown time was decreased in the stressful dry environment, but there was a significant sex‐by‐treatment interaction: at low humidity, females were more heat resistant than males, whereas at high humidity, the situation was reversed. Phenotypic variability of knockdown time was also lower in the dry environment. The magnitude of genetic correlation between the sexes at high humidity indicated genetic variation for sexual dimorphism in heat resistance. Heritability estimates based on one‐parent–offspring regressions tended to be higher under desiccation stress, and this could be explained by decreased environmental variance of heat resistance at low humidity. There was no indication that the additive genetic variance and evolvability of heat resistance differed between the environments. The pattern of heritability estimates suggests that populations of D. melanogaster may have a greater potential for evolving higher thermal tolerance under arid conditions.     

Variations in morphological and life-history traits under extreme temperatures in <Emphasis Type="Italic">Drosophila ananassae</Emphasis>

Using half-sib analysis, we analysed the consequences of extreme rearing temperatures on genetic and phenotypic variations in the morphological and life-history traits of Drosophila ananassae. Paternal half-sib covariance contains a relatively small proportion of the epistatic variance and lacks the dominance variance and variance due to maternal effect, which provides more reliable estimates of additive genetic variance. Experiments were performed on a mass culture population of D. ananassae collected from Kanniyakumari (India). Two extremely stressful temperatures (18°C and 32°C) and one standard temperature (25°C) were used to examine the effect of stressful and non-stressful environments on the morphological and life-history traits in males and females. Mean values of various morphological traits differed significantly among different temperature regimens in both males and females. Rearing at 18°C and 32°C resulted in decreased thorax length, wing-to-thorax (w/t) ratio, sternopleural bristle number, ovariole number, sex comb-tooth number and testis length. Phenotypic variances increased under stressful temperatures in comparison with non-stressful temperatures. Heritability and evolvability based on among-sires (males), among-dams (females), and the sum of the two components (sire + dam) showed higher values at both the stressful temperatures than at the non-stressful temperature. These differences reflect changes in additive genetic variance. Viability was greater at the high than the low extreme temperature. As viability is an indicator of stress, we can assume that stress was greater at 18°C than at 32°C in D. ananassae. The genetic variations for all the quantitative and life-history traits were higher at low temperature. Variation in sexual traits was more pronounced as compared with other morphometric traits, which shows that sexual traits are more prone to thermal stress. Our results agree with the hypothesis that genetic variation is increased in stressful environments.     

Multivariate genetic architecture of the Anolis dewlap reveals both shared and sex‐specific features of a sexually dimorphic ornament

Darwin viewed the ornamentation of females as an indirect consequence of sexual selection on males and the transmission of male phenotypes to females via the ‘laws of inheritance’. Although a number of studies have supported this view by demonstrating substantial between‐sex genetic covariance for ornament expression, the majority of this work has focused on avian plumage. Moreover, few studies have considered the genetic basis of ornaments from a multivariate perspective, which may be crucial for understanding the evolution of sex differences in general, and of complex ornaments in particular. Here, we provide a multivariate, quantitative‐genetic analysis of a sexually dimorphic ornament that has figured prominently in studies of sexual selection: the brightly coloured dewlap of Anolis lizards. Using data from a paternal half‐sibling breeding experiment in brown anoles (Anolis sagrei), we show that multiple aspects of dewlap size and colour exhibit significant heritability and a genetic variance–covariance structure ( G ) that is broadly similar in males ( G _m) and females ( G _f). Whereas sexually monomorphic aspects of the dewlap, such as hue, exhibit significant between‐sex genetic correlations (r_mf), sexually dimorphic features, such as area and brightness, exhibit reduced r_mf values that do not differ from zero. Using a modified random skewers analysis, we show that the between‐sex genetic variance–covariance matrix ( B) should not strongly constrain the independent responses of males and females to sexually antagonistic selection. Our microevolutionary analysis is in broad agreement with macroevolutionary perspectives indicating considerable scope for the independent evolution of coloration and ornamentation in males and females.     

Sex differences in the genetic architecture of aggressiveness in a sexually dimorphic spider

Sex differences in the genetic architecture of behavioral traits can offer critical insight into the processes of sex‐specific selection and sexual conflict dynamics. Here, we assess genetic variances and cross‐sex genetic correlations of two personality traits, aggression and activity, in a sexually size‐dimorphic spider, Nuctenea umbratica. Using a quantitative genetic approach, we show that both traits are heritable. Males have higher heritability estimates for aggressiveness compared to females, whereas the coefficient of additive genetic variation and evolvability did not differ between the sexes. Furthermore, we found sex differences in the coefficient of residual variance in aggressiveness with females exhibiting higher estimates. In contrast, the quantitative genetic estimates for activity suggest no significant differentiation between males and females. We interpret these results with caution as the estimates of additive genetic variances may be inflated by nonadditive genetic effects. The mean cross‐sex genetic correlations for aggression and activity were 0.5 and 0.6, respectively. Nonetheless, credible intervals of both estimates were broad, implying high uncertainty for these estimates. Future work using larger sample sizes would be needed to draw firmer conclusions on how sexual selection shapes sex differences in the genetic architecture of behavioral traits.     

Rapid reversal of a potentially constraining genetic covariance between leaf and flower traits in Silene latifolia

Genetic covariance between two traits generates correlated responses to selection, and may either enhance or constrain adaptation. Silene latifolia exhibits potentially constraining genetic covariance between specific leaf area (SLA) and flower number in males. Flower number is likely to increase via fecundity selection but the correlated increase in SLA increases mortality, and SLA is under selection to decrease in dry habitats. We selected on trait combinations in two selection lines for four generations to test whether genetic covariance could be reduced without significantly altering trait means. In one selection line, the genetic covariance changed sign and eigenstructure changed significantly, while in the other selection line eigenstructure remained similar to the control line. Changes in genetic variance–covariance structure are therefore possible without the introduction of new alleles, and the responses we observed suggest that founder effects and changes in frequency of alleles of major effect may be acting to produce the changes.     

SEXUAL CONFLICT AND THE MAINTENANCE OF MULTIVARIATE GENETIC VARIATION

Mate choice should erode additive genetic variation in sexual displays, yet these traits often harbor substantial genetic variation. Nevertheless, recent developments in quantitative genetics have suggested that multivariate genetic variation in the combinations of traits under selection may still be depleted. Accordingly, the erosion and maintenance of variation may only be detectable by studying whole suites of traits. One potential process favoring the maintenance of genetic variance in multiple trait combinations is the modification of sexual selection via sexually antagonistic interactions between males and females. Here we consider how interlocus sexual conflict can shape the genetic architecture of male sexual traits in the cricket, Teleogryllus commodus. In this species, the ability of each sex to manipulate insemination success significantly alters the selection acting on male courtship call properties. Using a quantitative genetic breeding design we estimated the additive genetic variation in these traits and then predicted the change in variation due to previously documented patterns of sexual selection. Our results indicate that female choice should indeed deplete multivariate genetic variance, but that sexual conflict over insemination success may oppose this loss of variance. We suggest that changes in the direction of selection due to sexually antagonistic interactions will be an important and potentially widespread factor in maintaining multivariate genetic variation.     

Genetic constraints and sexual dimorphism in immune defense

The absence of continued evolutionary change despite the presence of genetic variation and directional selection is very common. Genetic correlations between traits can reduce the evolvability of traits. One intriguing example might be found in a sexual conflict over sexually dimorphic traits: a common genetic architecture constrains the response to selection on a trait subjected to sexually asymmetric selection pressures. Here we show that males and females of the mealworm beetle Tenebrio molitor differ in the quantitative genetic architecture of four traits related to immune defense and condition. Moreover, high genetic correlations between the sexes constitute a genetic constraint to the evolution of sexual dimorphism in immune defense. Our results suggest a general mechanism by which sexual conflict can promote evolutionary stasis. We furthermore show negative genetic correlations, strong indications of trade-offs, between immune traits for two pairs of traits in females.     

Genetic effects on flight capacity in the beet armyworm,Spodoptera exigua (Lep., Noctuidae)

The beet armyworm, Spodoptera exigua, is an important migratory insect pest in tropical and subtropical regions worldwide. The current study investigated genetic variation in the flight capacity of both female and male moths, using a quantitative genetics approach. The offspring–parent regression showed that parents had a significant influence on the flight duration of offspring, and the heritability estimated as 0.302. The upward selection increased mean flight duration from 123.7 to 284.6 min in females and from 113.9 to 254.0 min in males during 8 h of flight test; by contrast, downward selection decreased it from 123.7 to 65.6 min in females and from 113.9 to 29.8 min in males, while it did not change significantly in either females or males of the control line over eight generations. The mean realized heritability was estimated as 0.432 based on upward selection but 0.130 on downward selection, suggesting the asymmetry of response to selection on flight capacity. Reciprocal crosses between the two selected lines confirmed the dominance of ‘long‐flying genes’ in the inheritance of flight capacity. A positive genetic correlation was found between increased flight duration and pupal weight. The presence of such additive genetic variance and covariance for flight capacity and the fitness trait, pupal weight, in the population of S. exigua may have underpinned the evolution of its migratory behaviour.     

Condition dependence and the maintenance of genetic variance in a sexually dimorphic black scavenger fly

The maintenance of genetic variation in traits under strong sexual selection is a longstanding problem in evolutionary biology. The genic capture model proposes that this problem can be explained by the evolution of condition dependence in exaggerated male traits. We tested the predictions that condition dependence should be more pronounced in male sexual traits and that genetic variance in expression of these traits should increase under stress as among‐genotype variation in overall condition is exposed. Genetic variance in female and nonsexual traits should, by contrast, be similar across environments as a result of stabilizing selection on trait expression. The relationship between the degree of sexual dimorphism, condition dependence and additive genetic variance (V_a) was assessed for two morphological traits (body size and relative fore femur width) affecting male mating success in the black scavenger fly Sepsis punctum (Diptera: Sepsidae) and for development time (a nonsexual trait often correlated with body size). We compared trait expression between the sexes for two cross‐continental populations that differ in degree of sexual dimorphism (Ottawa and Zurich). Condition dependence was indeed most pronounced in males of the strongly dimorphic Zurich population (males larger), and V_a was similar for males and females unless the trait was strongly sex specific and condition dependent. Contrary to prediction, however, V_a primarily increased under food limitation in both sexes, and genetic variance in fore femur width was low to nil, perhaps depleted by putatively strong sexual selection. Solely for body size of Zurich males, V_a increased more in males than females at limited food, in accordance with the predictions of the genic capture model. Overall therefore, quantitative genetic evidence in support of the model was inconsistent and weak at best.     

Intralocus sexual conflict and the genetic architecture of sexually dimorphic traits in Prochyliza xanthostoma (Diptera: Piophilidae)

Because homologous traits of males and females are likely to have a common genetic basis, sex-specific selection (often resulting from sexual selection on one sex) may generate an evolutionary tug-of-war known as intralocus sexual conflict, which will constrain the adaptive divergence of the sexes. Theory suggests that intralocus sexual conflict can be mitigated through reduction of the intersexual genetic correlation (rMF), predicting negative covariation between rMF and sexual dimorphism. In addition, recent work showed that selection should favor reduced expression of alleles inherited from the opposite-sex parent (intersexual inheritance) in traits subject to intralocus sexual conflict. For traits under sexual selection in males, this should be manifested either in reduced maternal heritability or, when conflict is severe, in reduced heritability through the opposite-sex parent in offspring of both sexes. However, because we do not know how far these hypothesized evolutionary responses can actually proceed, the importance of intralocus sexual conflict as a long-term constraint on adaptive evolution remains unclear. In this study, we investigated the genetic architecture of sexual and nonsexual morphological traits in Prochyliza xanthostoma. The lowest rMF and greatest dimorphism were exhibited by two sexual traits (head length and antenna length) and, among all traits, the degree of sexual dimorphism was correlated negatively with rMF. Moreover, sexual traits exhibited reduced maternal heritabilities, and the most strongly dimorphic sexual trait (antenna length) was heritable only through the same-sex parent in offspring of both sexes. Our results support theory and suggest that intralocus sexual conflict can be resolved substantially by genomic adaptation. Further work is required to identify the proximate mechanisms underlying these patterns.     

Direct versus indirect sexual selection: genetic basis of colour, size and recruitment in a wild bird

Indirect and direct models of sexual selection make different predictions regarding the quantitative genetic relationships between sexual ornaments and fitness. Indirect models predict that ornaments should have a high heritability and that strong positive genetic covariance should exist between fitness and the ornament. Direct models, on the other hand, make no such assumptions about the level of genetic variance in fitness and the ornament, and are therefore likely to be more important when environmental sources of variation are large. Here we test these predictions in a wild population of the blue tit (Parus caeruleus), a species in which plumage coloration has been shown to be under sexual selection. Using 3 years of cross-fostering data from over 250 breeding attempts, we partition the covariance between parental coloration and aspects of nestling fitness into a genetic and environmental component. Contrary to indirect models of sexual selection, but in agreement with direct models, we show that variation in coloration is only weakly heritable h2<0.11, and that two components of offspring fitness-nestling size and fledgling recruitment-are strongly dependent on parental effects, rather than genetic effects. Furthermore, there was no evidence of significant positive genetic covariation between parental colour and offspring traits. Contrary to direct benefit models, however, we find little evidence that variation in colour reliably indicates the level of parental care provided by either males or females. Taken together, these results indicate that the assumptions of indirect models of sexual selection are not supported by the genetic basis of the traits reported on here.     

Sex-specific trait architecture in a spider with sexual size dimorphism

Sexual dimorphism, or sex-specific trait expression, may evolve when selection favours different optima for the same trait between sexes, that is, under antagonistic selection. Intra-locus sexual conflict exists when the sexually dimorphic trait under antagonistic selection is based on genes shared between sexes. A common assumption is that the presence of sexual-size dimorphism (SSD) indicates that sexual conflict has been, at least partly, resolved via decoupling of the trait architecture between sexes. However, whether and how decoupling of the trait architecture between sexes has been realized often remains unknown. We tested for differences in architecture of adult body size between sexes in a species with extreme SSD, the African hermit spider (Nephilingis cruentata), where adult female body size greatly exceeds that of males. Specifically, we estimated the sex-specific importance of genetic and maternal effects on adult body size among individuals that we laboratory-reared for up to eight generations. Quantitative genetic model estimates indicated that size variation in females is to a larger extent explained by direct genetic effects than by maternal effects, but in males to a larger extent by maternal than by genetic effects. We conclude that this sex-specific body-size architecture enables body-size evolution to proceed much more independently than under a common architecture to both sexes.     

THE QUANTITATIVE GENETICS AND COEVOLUTION OF MALE AND FEMALE REPRODUCTIVE TRAITS

Studies of experimental sexual selection have tested the effect of variation in the intensity of sexual selection on male investment in reproduction, particularly sperm. However, in several species, including Drosophila pseudoobscura, no sperm response to experimental evolution has occurred. Here, we take a quantitative genetics approach to examine whether genetic constraints explain the limited evolutionary response. We quantified direct and indirect genetic variation, and genetic correlations within and between the sexes, in experimental populations of D. pseudoobscura. We found that sperm number may be limited by low heritability and evolvability whereas sperm quality (length) has moderate V_A and CV_A but does not evolve. Likewise, the female reproductive tract, suggested to drive the evolution of sperm, did not respond to experimental sexual selection even though there was sufficient genetic variation. The lack of genetic correlations between the sexes supports the opportunity for sexual conflict over investment in sperm by males and their storage by females. Our results suggest no absolute constraint arising from a lack of direct or indirect genetic variation or patterns of genetic covariation. These patterns show why responses to experimental evolution are hard to predict, and why research on genetic variation underlying interacting reproductive traits is needed.     

ENVIRONMENT-DEPENDENCE OF QUANTITATIVE GENETIC PARAMETERS IN IMPATIENS PALLIDA

Population response to selection depends on the presence of additive genetic variance for traits under selection. When a population enters an alien environment, environment-induced changes in the expression of genetic variance may occur. These could have large effects on the response to selection. To investigate the environment-dependence of genetic variance, we conducted a reciprocal transplant experiment between two ecotypically differentiated populations of Impatiens pallida using the progeny of a standard mating design. The floodplain site was characterized by high water availability, moderate temperatures, and continuous dense stands of Impatiens. The hillside site was drier, with larger temperature extremes and supported only scattered patches of Impatiens with significantly lower seed production and earlier mortality. Estimates of heritability were low for each of the 13 traits measured in each population and site (range from 0–28%). Additive genetic variance for life-history traits tended to be larger than for morphological traits, but genetic variance in fitness was estimated to be not significantly different from zero in all cases. Significant heritability was detected in both populations for one trait (date of first cleistogamous flower) known to be closely related to fitness on the hillside. In general, heritability was reduced for populations when grown in the hillside site relative to the floodplain site, suggesting that stress acts to reduce the expression of genetic variance and the potential to respond to selection there. Consistent reductions in heritability associated with more stressful environments suggest that populations invading such sites may undergo little adaptive differentiation and be more prone to local extinction.     

Basal metabolic rate can evolve independently of morphological and behavioural traits

Quantitative genetic analyses of basal metabolic rate (BMR) can inform us about the evolvability of the trait by providing estimates of heritability, and also of genetic correlations with other traits that may constrain the ability of BMR to respond to selection. Here, we studied a captive population of zebra finches (Taeniopygia guttata) in which selection lines for male courtship rate have been established. We measure BMR in these lines to see whether selection on male sexual activity would change BMR as a potentially correlated trait. We find that the genetic correlation between courtship rate and BMR is practically zero, indicating that the two traits can evolve independently of each other. Interestingly, we find that the heritability of BMR in our population (h²=0.45) is markedly higher than was previously reported for a captive zebra finch population from Norway. A comparison of the two studies shows that additive genetic variance in BMR has been largely depleted in the Norwegian population, especially the genetic variance in BMR that is independent of body mass. In our population, the slope of BMR increase with body mass differs not only between the sexes but also between the six selection lines, which we tentatively attribute to genetic drift and/or founder effects being strong in small populations. Our study therefore highlights two things. First, the evolvability of BMR may be less constrained by genetic correlations and lack of independent genetic variation than previously described. Second, genetic drift in small populations can rapidly lead to different evolvabilities across populations.     

SEXUAL SELECTION IN THE BARN SWALLOW HIRUNDO RUSTICA. III. FEMALE TAIL ORNAMENTS

Male secondary sexual characters are often expressed in females, and the maintenance of the character in females can be due to either direct selection on females favoring the maintenance of the trait, or a correlated response to selection in males. Here I report on determinants of and phenotypic selection on tail length of female barn swallows Hirundo rustica. The homologous trait in males is under strong directional sexual selection. Female tail length was positively associated with several reproductive parameters including total seasonal reproductive success, even when controlling for year and age effects. A change in female tail length from one year to another was often associated with a change in the reproductive parameters correlated with absolute tail length. There was little evidence for an association between female tail length and the duration of the incubation period (only females incubate) and absolute and relative female provisioning rates of offspring, and subsequent size of offspring. Tail length of female barn swallows was positively correlated with that of their mates. Female tail length was a heritable trait as determined from regression of the tail trait of offspring on that of their mother and their father, and there was a positive genetic correlation between the tail trait in males and females. In conclusion, female tail length reliably reflects female reproductive potential, and the trait appears to be under directional selection, which may result in an evolutionary response to selection because of the heritability of the tail trait.     

Multivariate quantitative genetics and the lek paradox: genetic variance in male sexually selected traits of Drosophila serrata under field conditions

Single male sexually selected traits have been found to exhibit substantial genetic variance, even though natural and sexual selection are predicted to deplete genetic variance in these traits. We tested whether genetic variance in multiple male display traits of Drosophila serrata was maintained under field conditions. A breeding design involving 300 field-reared males and their laboratory-reared offspring allowed the estimation of the genetic variance-covariance matrix for six male cuticular hydrocarbons (CHCs) under field conditions. Despite individual CHCs displaying substantial genetic variance under field conditions, the vast majority of genetic variance in CHCs was not closely associated with the direction of sexual selection measured on field phenotypes. Relative concentrations of three CHCs correlated positively with body size in the field, but not under laboratory conditions, suggesting condition-dependent expression of CHCs under field conditions. Therefore condition dependence may not maintain genetic variance in preferred combinations of male CHCs under field conditions, suggesting that the large mutational target supplied by the evolution of condition dependence may not provide a solution to the lek paradox in this species. Sustained sexual selection may be adequate to deplete genetic variance in the direction of selection, perhaps as a consequence of the low rate of favorable mutations expected in multiple trait systems.     

THE GENOMIC ARCHITECTURE OF SEXUAL DIMORPHISM IN THE DIOECIOUS PLANT SILENE LATIFOLIA

Evaluating the genetic architecture of sexual dimorphism can aid our understanding of the extent to which shared genetic control of trait variation versus sex‐specific control impacts the evolutionary dynamics of phenotypic change within each sex. We performed a QTL analysis on Silene latifolia to evaluate the contribution of sex‐specific QTL to phenotypic variation in 46 traits, whether traits involved in trade‐offs had colocalized QTL, and whether the distribution of sex‐specific loci can explain differences between the sexes in their variance/covariance matrices. We used a backcross generation derived from two artificial‐selection lines. We found that sex‐specific QTL explained a significantly greater percent of the variation in sexually dimorphic traits than loci expressed in both sexes. Genetically correlated traits often had colocalized QTL, whose signs were in the expected direction. Lastly, traits with different genetic correlations within the sexes displayed a disproportionately high number of sex‐specific QTL, and more QTL co‐occurred in males than females, suggesting greater trait integration. These results show that sex differences in QTL patterns are congruent with theory on the resolution of sexual conflict and differences based on G ‐matrix results. They also suggest that trade‐offs and trait integration are likely to affect males more than females.     

Male-limited evolution suggests no extant intralocus sexual conflict over the sexually dimorphic cuticular hydrocarbons of <Emphasis Type="Italic">Drosophila melanogaster</Emphasis>

Sexually dimorphic traits are likely to have evolved through sexually antagonistic selection. However, recent empirical data suggest that intralocus sexual conflict often persists, even when traits have diverged between males and females. This implies that evolved dimorphism is often incomplete in resolving intralocus conflict, providing a mechanism for the maintenance of genetic variance in fitness-related traits. We used experimental evolution in Drosophila melanogaster to directly test for ongoing conflict over a suite of sexually dimorphic cuticular hydrocarbons (CHCs) that are likely targets of sex-specific selection. Using a set of experimental populations in which the transmission of genetic material had been restricted to males for 82 generations, we show that CHCs did not evolve, providing experimental evidence for the absence of current intralocus sexual conflict over these traits. The absence of ongoing conflict could indicate that CHCs have never been the target of sexually antagonistic selection, although this would require the existing dimorphism to have evolved via completely sexlinked mutations or as a result of former, but now absent, pleiotropic effects of the underlying loci on another trait under sexually antagonistic selection. An alternative interpretation, and which we believe to be more likely, is that the extensive CHC sexual dimorphism is the result of past intralocus sexual conflict that has been fully resolved, implying that these traits have evolved genetic independence between the sexes and that genetic variation in them is therefore maintained by alternative mechanisms. This latter interpretation is consistent with the known roles of CHCs in sexual communication in this species and with previous studies suggesting the genetic independence of CHCs between males and females. Nevertheless, direct estimates of sexually antagonistic selection will be important to fully resolve these alternatives.     

The effect of trait type and strength of selection on heritability and evolvability in an island bird population

The heritability (h²) of fitness traits is often low. Although this has been attributed to directional selection having eroded genetic variation in direct proportion to the strength of selection, heritability does not necessarily reflect a trait's additive genetic variance and evolutionary potential (“evolvability”). Recent studies suggest that the low h² of fitness traits in wild populations is caused not by a paucity of additive genetic variance (V_A) but by greater environmental or nonadditive genetic variance (V_R). We examined the relationship between h² and variance‐standardized selection intensities (i or β_σ), and between evolvability (I_A:V_A divided by squared phenotypic trait mean) and mean‐standardized selection gradients (β_μ). Using 24 years of data from an island population of Savannah sparrows, we show that, across diverse traits, h² declines with the strength of selection, whereas I_A and I_R (V_R divided by squared trait mean) are independent of the strength of selection. Within trait types (morphological, reproductive, life‐history), h², I_A, and I_R are all independent of the strength of selection. This indicates that certain traits have low heritability because of increased residual variance due to the age at which they are expressed or the multiple factors influencing their expression, rather than their association with fitness.