Resistance to temperature extremes between and within life cycle stages in Drosophila serrata, D-birchii and their hybrids: intraspecific and interspecific comparisons

Intraspecific Drosophila studies suggest that resistance to heal and cold stresses are largely independent and that correlations across life cycle stages are low whereas comparisons of Drosophila species indicate correlations between heat and cold resistance as well as between resistance levels in different life cycle stages. These inconsistent results may reflect differences in associations among traits at the interspecific and intraspecific levels or interspecific correlations arising because of correlated selection pressures. These alternatives were tested using Drosophila serrata, D. birchii and hybrids derived from these species. Variation among hybrid lines and families was used to test associations at the interspecific level while intraspecific variation was examined using isofemale lines of D. serrata. There was a significant association between adult heat knockdown time at 38 degreesC and adult cold resistance in one set of hybrid lines. An association between female knockdown resistance to heat and larval heat resistance was also evident in one set of hybrids. Resistance to heat anti cold at the larval stage were not correlated at either the intraspecific or interspecific levels. At the intraspecific level, lan al heat resistance and two measures of adult heat resistance were uncorrelated. Moreover, adult and larval cold resistance measures were not correlated at either the intraspecific or interspecific levels. These results suggest that there are no associations between resistance to heat and cold extremes and that extreme temperature resistance is largely independent across life cycle stages at both the intraspecific and interspecific levels. Species associations may therefore arise from correlated selection pressures rather than trait correlations. (C) 2000 The Linnean Society of London.

Evolutionary experiments on mate recognition in the Drosophila serrata species complex

It is becoming increasingly apparent that at least some aspects of the evolution of mate recognition may be amenable to manipulation in evolutionary experiments. Quantitative genetic analyses that focus on the genetic consequences of evolutionary processes that result in mate recognition evolution may eventually provide an understanding of the genetic basis of the process of speciation. We review a series of experiments that have attempted to determine the genetic basis of the response to natural and sexual selection on mate recognition in the Drosophila serrata species complex. The genetic basis of mate recognition has been investigated at three levels: (1) between the species of D. serrata and D. birchii using interspecific hybrids, (2) between populations of D. serrata that are sympatric and allopatric with respect to D. birchii, and (3) within populations of D. serrata. These experiments suggest that it may be possible to use evolutionary experiments to observe important events such as the reinforcement of mate recognition, or the generation of the genetic associations that are central to many sexual selection models.

Evolution of additive and nonadditive genetic variance in development time along a cline in Drosophila serrata

Latitudinal clines provide natural systems that may allow the effect of natural selection on the genetic variance to be determined. Ten clinal populations of Drosophila serrata collected from the eastern coast of Australia were used to examine clinal patterns in the trait mean and genetic variance of the life-history trait egg-to-adult development time. Development time significantly lengthened from tropical areas to temperate areas. The additive genetic variance for development time in each population was not associated with latitude but was associated with the population mean development time. Additive genetic variance tended to be larger in populations with more extreme development times and appeared to be consistent with allele frequency change. In contrast, the nonadditive genetic variance was not associated with the population mean but was associated with latitude. Levels of nonadditive genetic variance were greatest in the region of the cline where the gradient in the change in mean was greatest, consistent with Barton's (1999) conjecture that the generation of linkage disequilibrium may become an important component of the genetic variance in systems with a spatially varying optimum.

Signal trait sexual dimorphism and mutual sexual selection in Drosophila serrata

The evolution of sexual dimorphism may occur when natural and sexual selection result in different optimum trait values for males and females. Perhaps the most prominent examples of sexual dimorphism occur in sexually selected traits, for which males usually display exaggerated trait levels, while females may show reduced expression of the trait. In some species, females also exhibit secondary sexual traits that may either be a consequence of a correlated response to sexual selection on males or direct sexual selection for female secondary sexual traits. In this experiment, we simultaneously measure the intersex genetic correlations and the relative strength of sexual selection on males and females for a set of cuticular hydrocarbons in Drosophila serrata. There was significant directional sexual selection on both male and female cuticular hydrocarbons: the strength of sexual selection did not differ among the sexes but males and females preferred different cuticular hydrocarbons. In contrast with many previous studies of sexual dimorphism, intersex genetic correlations were low. The evolution of sexual dimorphism in D. serrata appears to have been achieved by sex-limited expression of traits controlled by genes on the X chromosome and is likely to be in its final stages.

The genetic covariance among clinal environments after adaptation to an environmental gradient in Drosophila serrata

We examined the genetic basis of clinal adaptation by determining the evolutionary response of life-history traits to laboratory natural selection along a gradient of thermal stress in Drosophila serrata. A gradient of heat stress was created by exposing larvae to a heat stress of 36degrees for 4 hr for 0, 1, 2, 3, 4, or 5 days of larval development, with the remainder of development taking place at 25degrees. Replicated lines were exposed to each level of this stress every second generation for 30 generations. At the end of selection, we conducted a complete reciprocal transfer experiment where all populations were raised in all environments, to estimate the realized additive genetic covariance matrix among clinal environments in three life-history traits. Visualization of the genetic covariance functions of the life-history traits revealed that the genetic correlation between environments generally declined as environments became more different and even became negative between the most different environments in some cases. One exception to this general pattern was a life-history trait representing the classic trade-off between development time and body size, which responded to selection in a similar genetic fashion across all environments. Adaptation to clinal environments may involve a number of distinct genetic effects along the length of the cline, the complexity of which may not be fully revealed by focusing primarily on populations at the ends of the cline.

Multivariate quantitative genetics and the Lek Paradox: Genetic variance in male sexually selected traits of Drosophila serrata under field control

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.

Contrasting mutual sexual selection on homologous signal traits in Drosophila serrata

The nature of male mating preferences, and how they differ from female mating preferences in species with conventional sex roles, has received little attention in sexual selection studies. We estimated the form and strength of sexual selection as a consequence of male and female mating preferences in a laboratory-based population of Drosophila serrata. The differences between sexual selection on male and female signal traits (cuticular hydrocarbons [CHCs]) were evaluated within a formal framework of linear and nonlinear selection gradients. Females tended to exert linear sexual selection on male CHCs, whereas males preferred intermediate female CHC phenotypes leading to convex (stabilizing) selection gradients. Possible mechanisms determining the nonlinear nature of sexual selection on female CHCs are proposed.

Age determination in individual wild-caught Drosophila serrata using pteridine concentration

Fluorescence spectrophotometry can reliably detect levels of the pteridine 6-biopterin in the heads of individual Drosophila serrata Malloch 1927. Pteridine content in both laboratory and field captured flies is typically a level of magnitude higher than the minimally detectable level (mean(lab)=0.54 units, mean(field)=0.44 units, minimum detectable level=0.01 units) and can be used to predict individual age in laboratory populations with high certainty (r(2)=57%). Laboratory studies of individuals of known age ( from 1 to 48 days old) indicate that while pteridine level increases linearly with age, they also increase in a linear manner with rearing temperature and ambient light levels, but are independent of sex. As expected, the longevity of laboratory-reared males ( at least 48 days) is higher than the range of predicted ages of wild-caught males based on individual pteridine levels (40 days). However, the predictive equation based on pteridine level alone suggested that a number of wild-caught males were less than 0 days old, and the 95% confidence for these predictions based on the inverse regression broad. The age of the oldest wild-caught male is to fall within the range of 2 to 50 days. The effects of temperature and light intensity determined in laboratory study (effect sizes omega(2)=14.3 and respectively) suggests that the calibration of the prediction equation for field populations would significantly improved when combined with fine scaled studies of habitat temperature and light conditions. ability to determine relative age in individual wild-caught D. serrata presents great opportunities for a variety evolutionary studies on the dynamics of populations.

Measuring natural and sexual selection on breeding values of male display traits in Drosophila serrata

Fundamental to many theories of sexual selection is the expectation that sexual traits, which males use in an attempt to increase mating success, confer costs as well as benefits to individual males. Although evolution of exaggerated male traits is predicted to be halted, by costs applied by natural selection, there is a lack of empirical work devoted to quantitatively establishing whether natural selection opposes sexual selection generated by the preferences of females. In this study, we quantified natural and sexual selection gradients on breeding values for cuticular hydrocarbon (CHC) components of male contact pheromones in Drosophila serrata. As male sexual traits may often be environmentally condition dependent, breeding values were used in the selection analysis to remove the possibility of environmental correlations between the measured trait and fitness biasing estimates of selection. The direction of natural selection was found to oppose sexual selection on a subset of CHCs examined. Opposing natural and sexual selection suggests that further evolution of the male pheromone may in part be limited by costs associated with attractive male CHC blends.

Cuticular hydrocarbons of Drosophila birchii and D-serrata: Identification and role in mate choice in D-serrata

The cuticular hydrocarbon compositions of two sympatric species of Australian Drosophila in the montium subgroup of the melanogaster group that use cuticular hydrocarbons in mate recognition have been characterized. Drosophila birchii has 34 components in greater than trace amounts, with a carbon number range of C-20 to C-33. Drosophila serrata has 21 components above trace level and a carbon number range of C-24 to C-31. These two species share eight hydrocarbon components, with all but two of them being monoenes. For both species, the (Z)-9-monoenes are the predominant positional isomer. The hydrocarbons of D. birchii are n-alkanes, n-alkenes (Z)-5-, (Z)-7-, (Z)-9-, and (Z)-11-), low to trace levels of homologous (Z,Z)-7,11- and (Z,Z)-9,13-dienes; and trace amounts of (Z,Z)-5,9- C-25:2, a major component of D. serrata. Only one methyl branched hydrocarbon was detected (2-methyl C-28), and it occurred at very low levels. The hydrocarbons of D. serrata are dominated by a homologous series of (Z,Z)-5,9-dienes, and notably, are characterized by the apparent absence of n-alkanes. Homologous series of (Z)-5-, (Z)-7-, and (Z)-9- alkenes are also present in D. serrata as well as 2-methyl alkanes. Drosophila serrata females display strong directional mate choice based on male cuticular hydrocarbons and prefer D. serrata males with higher relative abundances of the 2-methyl alkanes, but lower relative abundances of (Z,Z)-5,9- C-24:2 and (Z)-9-C-25:1.

Evolution of a mate recognition system after hybridization between two Drosophila species

I investigated the genetic relationship between male and female components of the mate recognition system and how this relationship influenced the subsequent evolution of the two traits, in a series of replicate populations of interspecific hybrids. Thirty populations of hybrids between Drosophila serrata and Drosophila birchii were established and maintained for 24 generations. At the fifth generation after hybridization, the mating success of hybrid individuals with the D. serrata parent was determined. The genetic correlation between male and female components of the male recognition system, as a consequence of pleiotropy or tight physical linkage, was found to be significant but low (r = 0.388). This result suggested that pleiotropy may play only a minor role in the evolution of mate recognition in this system. At the twenty-fourth generation after hybridization, the mating success of the hybrids was again determined. The evolution of male and female components was investigated by analyzing the direction of evolution of each hybrid line with respect to its initial position in relation to the genetic regression. Male and female components appeared to converge on a single equilibrium point, rather than evolving along trajectories with slope equal to the genetic regression, toward a line of equilibria.

Levels of mate recognition within and between two Drosophila species and their hybrids

If sexual selection is to result in speciation, traits involved in mate choice within species need to be capable of producing sexual isolation between species. We investigated the association between mate choice and sexual isolation using interspecific hybrids between two sibling species, Drosophila serrata and Drosophila birchii. A perfuming experiment demonstrated that olfaction was involved in the sexual isolation between the two species. A quantitative genetic analysis using 30 populations of hybrids between the two species indicated that mating success in hybrid individuals was predominately determined by cuticular hydrocarbons; the average genetic correlation between mating success and cuticular hydrocarbon profile was 0.84, and in some instances exceeded 0.95. Multivariate analysis of the cuticular hydrocarbons of the two species revealed that there were three independent blends of cuticular hydrocarbons that separated three levels of organization: species, sex, and sex within species. The hydrocarbons used by hybrids in mate choice included those that separated the two species, demonstrating that species-specific characters may be used in mate choice within populations. The interspecific reciprocal cross had a major effect on which cuticular hydrocarbons were associated with mating success, indicating that the expression of the cuticular hydrocarbons was strongly sex linked.

Evolution of the genetic covariance between male and female components of mate recognition: An experimental test

The evolution of a positive genetic correlation between male and female components of mate recognition systems will result as a consequence of assortative mating and, in particular, is central to a number of theories of sexual selection. Although the existence of such genetic correlations has been investigated in a number of taxa, it has yet to be shown that such correlations evolve and whether they may evolve as rapidly as suggested by sexual selection models. In this study, I used a hybridization experiment to disrupt natural mate recognition systems and then observed the subsequent evolutionary dynamics of the genetic correlation between male and female components for 56 generations in hybrids between Drosophila serrata and Drosophila birchii. The genetic correlation between male and female components evolved from 0.388 at generation 5 to 1.017 at generation 37 and then declined to -0.040 after a further 19 generations. These results indicated that the genetic basis of the mate recognition system in the hybrid populations evolved rapidly. The initial rapid increase in the genetic correlation was consistent with the classic assumption that male and female components will coevolve under sexual selection. The subsequent decline in genetic correlation may be attributable to the fixation of major genes or, alternatively, may be a result of a cyclic evolutionary change in mate recognition.

Positive genetic correlation between female preference and offspring fitness

In many species, females display preferences for extreme male signal traits, but it has not been determined if such preferences evolve as a consequence of females gaining genetic benefits from exercising choice. If females prefer extreme male traits because they indicate male genetic quality that will enhance the fitness of offspring, a genetic correlation will evolve between female preference genes and genes that confer offspring fitness. We show that females of Drosophila serrata prefer extreme male cuticular hydrocarbon (CHC) blends, and that this preference affects offspring fitness. Female preference is positively genetically correlated with offspring fitness, indicating that females have gained genetic benefits from their choice of males. Despite male CHCs experiencing strong sexual selection, the genes underlying attractive CHCs also conferred lower offspring fitness, suggesting a balance between sexual selection and natural selection may have been reached in this population.

Genetic constraints on the evolution of mate recognition under natural selection

Field populations of Drosophila serrata display reproductive character displacement in cuticular hydrocarbons (CHCs) when sympatric with Drosophila birchii. We have previously shown that the naturally occurring pattern of reproductive character displacement can be experimentally replicated by exposing field allopatric populations of D. serrata to experimental sympatry with D. birchii. Here, we tested whether the repeated evolution of reproductive character displacement in natural and experimental populations was a consequence of genetic constraints on the evolution of CHCs. The genetic variance-covariance (G) matrices for CHCs were determined for populations of D. serrata that had evolved in either the presence or absence of D. birchii under field and experimental conditions. Natural selection on mate recognition under both field and experimental sympatric conditions increased the genetic variance in CHCs consistent with a response to selection based on rare alleles. A close association between G eigenstructure and the eigenstructure of the phenotypic divergence (D) matrix in natural and experimental populations suggested that G matrix eigenstructure may have determined the direction in which reproductive character displacement evolved during the reinforcement of mate recognition.