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ABSTRACT: Although adaptive change is usually associated with complex changes in phenotype, few genetic investigations have been conducted on adaptations that involve sets of high-dimensional traits. Microarrays have supplied high-dimensional descriptions of gene expression, and phenotypic change resulting from adaptation often results in large-scale changes in gene expression. We demonstrate how genetic analysis of large-scale changes in gene expression generated during adaptation can be accomplished by determining high-dimensional variance partitioning within classical genetic experimental designs. A microarray experiment conducted on a panel of recombinant inbred lines (RILs) generated from two populations of Drosophila serrata that have diverged in response to natural selection, revealed genetic divergence in 10.6% of 3762 gene products examined. Over 97% of the genetic divergence in transcript abundance was explained by only 12 genetic modules. The two most important modules, explaining 50% of the genetic variance in transcript abundance, were genetically correlated with the morphological traits that are known to be under selection. The expression of three candidate genes from these two important genetic modules was assessed in an independent experiment using qRT-PCR on 430 individuals from the panel of RILs, and confirmed the genetic association between transcript abundance and morphological traits under selection.
Evolution 11/2011; 65(11):3126-37. · 5.15 Impact Factor
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ABSTRACT: Mutual mate choice for homologous sexual display traits has been demonstrated in several recent studies yet little attention has been given to quantitative comparison of the strength and form of mate preferences between the sexes. Such comparisons may provide important insight into the evolution of mate choice for honest signals. In particular, because females generally provide the majority of resources for initial offspring development, female displays may trade-off with fecundity, causing preference evolution to differ between the sexes. Recent theory suggests that adaptive male preferences for honest displays in females are possible under certain conditions and may result in preferences that are convex (i.e., stabilizing) in form. We compared sexual selection on a suite of contact pheromones arising from mutual mate choice using nine separate geographic populations of Drosophila serrata. We show that the convex selection is stronger on females than on males overall in these populations, and that convex selection is the predominate form of nonlinear selection on females but not males.
Evolution 03/2011; 65(3):893-9. · 5.15 Impact Factor
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ABSTRACT: Organisms adjust to seasonal variability in the environment by responding to cues that indicate environmental change. As most studies of seasonal phenotypic plasticity test only the effect of a single environmental cue, how animals may integrate information from multiple cues to fine-tune plastic responses remains largely unknown. We examined the interaction between correlated (seasonally matching) and conflicting (seasonally opposite) temperature and photoperiod cues on the acclimation of performance traits in male zebrafish, Danio rerio. We acclimated fish for 8 weeks and then tested the change in thermal dependence of maximum burst swimming and feeding rate between 8 and 38°C. We predicted that correlated environmental cues should induce a greater acclimation response than uncorrelated cues. However, we found that only temperature was important for the seasonal acclimation of performance traits in zebrafish. Thermal acclimation shifted the thermal performance curve of both traits. For maximum burst swimming, performance increased for each group near the acclimation temperature and reduced in environments that were far from their acclimation temperature. The feeding rate of cold-acclimated zebrafish was reduced across the test temperature range compared with that of warm-acclimated fish. Our study is the first that has found no effect of the covariation between temperature and photoperiod acclimation cues on locomotor performance in fishes. Our results support the intuitive idea that photoperiod may be a less important seasonal cue for animals living at lower latitudes.
Journal of Experimental Biology 11/2010; 213(Pt 21):3705-9. · 3.00 Impact Factor
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ABSTRACT: Indirect genetics effects (IGEs)--when the genotype of one individual affects the phenotypic expression of a trait in another--may alter evolutionary trajectories beyond that predicted by standard quantitative genetic theory as a consequence of genotypic evolution of the social environment. For IGEs to occur, the trait of interest must respond to one or more indicator traits in interacting conspecifics. In quantitative genetic models of IGEs, these responses (reaction norms) are termed interaction effect coefficients and are represented by the parameter psi (Psi). The extent to which Psi exhibits genetic variation within a population, and may therefore itself evolve, is unknown. Using an experimental evolution approach, we provide evidence for a genetic basis to the phenotypic response caused by IGEs on sexual display traits in Drosophila serrata. We show that evolution of the response is affected by sexual but not natural selection when flies adapt to a novel environment. Our results indicate a further mechanism by which IGEs can alter evolutionary trajectories--the evolution of interaction effects themselves.
Evolution 06/2010; 64(6):1849-56. · 5.15 Impact Factor
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ABSTRACT: We took a comparative approach utilizing clines to investigate the extent to which natural selection may have shaped population divergence in cuticular hydrocarbons (CHCs) that are also under sexual selection in Drosophila. We detected the presence of CHC clines along a latitudinal gradient on the east coast of Australia in two fly species with independent phylogenetic and population histories, suggesting adaptation to shared abiotic factors. For both species, significant associations were detected between clinal variation in CHCs and temperature variation along the gradient, suggesting temperature maxima as a candidate abiotic factor shaping CHC variation among populations. However, rainfall and humidity correlated with CHC variation to differing extents in the two species, suggesting that response to these abiotic factors may vary in a species-specific manner. Our results suggest that natural selection, in addition to sexual selection, plays a significant role in structuring among-population variation in sexually selected traits in Drosophila.
Evolution 06/2010; 64(6):1784-94. · 5.15 Impact Factor
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ABSTRACT: Although divergent natural selection is common in nature, the extent to which genetic constraints bias evolutionary trajectories in its presence remains largely unknown. Here we develop a general framework to integrate estimates of divergent selection and genetic constraints to estimate their contributions to phenotypic divergence among natural populations. We apply these methods to estimates of phenotypic selection and genetic covariance from sexually selected traits that have undergone adaptive divergence among nine natural populations of the fly Drosophila serrata. Despite ongoing sexual selection within populations, differences in its direction among them, and genetic variance for all traits in all populations, divergent sexual selection only weakly resembled the observed pattern of divergence. Accounting for the influence of genetic covariance among the traits significantly improved the alignment between observed and predicted divergence. Our results suggest that the direction in which sexual selection generates divergence may depend on the pattern of genetic constraint in individual populations, ultimately restricting how sexually selected traits may diversify. More generally, we show how evolution is likely to proceed in the direction of major axes of genetic variance, rather than the direction of selection itself, when genetic variance-covariance matrices are ill conditioned and genetic variance is low in the direction of selection.
The American Naturalist 02/2010; 175(2):186-96. · 4.72 Impact Factor
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ABSTRACT: Determining how genetic variance changes under selection in natural populations has proved to be a very resilient problem in evolutionary genetics. In the same way that understanding the availability of genetic variance within populations requires the simultaneous consideration of genetic variance in sets of functionally related traits, determining how genetic variance changes under selection in natural populations will require ascertaining how genetic variance-covariance (G) matrices evolve. Here, we develop a geometric framework using higher-order tensors, which enables the empirical characterization of how G matrices have diverged among populations. We then show how divergence among populations in genetic covariance structure can then be associated with divergence in selection acting on those traits using key equations from evolutionary theory. Using estimates of G matrices of eight male sexually selected traits from nine geographical populations of Drosophila serrata, we show that much of the divergence in genetic variance occurred in a single trait combination, a conclusion that could not have been reached by examining variation among the individual elements of the nine G matrices. Divergence in G was primarily in the direction of the major axes of genetic variance within populations, suggesting that genetic drift may be a major cause of divergence in genetic variance among these populations.
Philosophical Transactions of The Royal Society B Biological Sciences 07/2009; 364(1523):1567-78. · 6.40 Impact Factor
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ABSTRACT: Drosophila harbor substantial genetic variation for antibacterial defense, and investment in immunity is thought to involve a costly trade-off with life history traits, including development, life span, and reproduction. To understand the way in which insects invest in fighting bacterial infection, we selected for survival following systemic infection with the opportunistic pathogen Pseudomonas aeruginosa in wild-caught Drosophila melanogaster over 10 generations. We then examined genome-wide changes in expression in the selected flies relative to unselected controls, both of which had been infected with the pathogen. This powerful combination of techniques allowed us to specifically identify the genetic basis of the evolved immune response. In response to selection, population-level survivorship to infection increased from 15% to 70%. The evolved capacity for defense was costly, however, as evidenced by reduced longevity and larval viability and a rapid loss of the trait once selection pressure was removed. Counter to expectation, we observed more rapid developmental rates in the selected flies. Selection-associated changes in expression of genes with dual involvement in developmental and immune pathways suggest pleiotropy as a possible mechanism for the positive correlation. We also found that both the Toll and the Imd pathways work synergistically to limit infectivity and that cellular immunity plays a more critical role in overcoming P. aeruginosa infection than previously reported. This work reveals novel pathways by which Drosophila can survive infection with a virulent pathogen that may be rare in wild populations, however, due to their cost.
PLoS Pathogens 05/2009; 5(4):e1000385. · 9.13 Impact Factor
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ABSTRACT: We develop expressions for the power to detect associations between parental genotypes and offspring phenotypes for quantitative traits. Three different "indirect" experimental designs are considered: full-sib, half-sib, and full-sib-half-sib families. We compare the power of these designs to detect genotype-phenotype associations relative to the common, "direct," approach of genotyping and phenotyping the same individuals. When heritability is low, the indirect designs can outperform the direct method. However, the extra power comes at a cost due to an increased phenotyping effort. By developing expressions for optimal experimental designs given the cost of phenotyping relative to genotyping, we show how the extra costs associated with phenotyping a large number of individuals will influence experimental design decisions. Our results suggest that indirect association studies can be a powerful means of detecting allelic associations in outbred populations of species for which genotyping and phenotyping the same individuals is impractical and for life history and behavioral traits that are heavily influenced by environmental variance and therefore best measured on groups of individuals. Indirect association studies are likely to be favored only on purely economical grounds, however, when phenotyping is substantially less expensive than genotyping. A web-based application implementing our expressions has been developed to aid in the design of indirect association studies.
Genetics 01/2009; 181(2):755-65. · 4.01 Impact Factor
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ABSTRACT: The Q(ST)-F(ST) comparison has become an increasingly common method for inferring adaptive quantitative trait divergence among populations. For cases in which there is divergence in multiple traits, most studies have applied the method by performing multiple univariate Q(ST)-F(ST) comparisons. However, because traits are often genetically correlated, such univariate analyses are likely to paint a simplified picture of adaptive divergence. Here we show how the multivariate analogue of Q(ST), F(STq), which accounts for genetic correlations among traits, can be used to supply a more detailed picture of multitrait divergence. We apply the method to naturally occurring genetic variation for a suite of sexually selected display traits in Drosophila serrata. The analyses suggest the operation of divergent multivariate selection that has influenced multiple independent axes of genetic variance in a sex-specific manner. Finally, we show how a comparison of the components of F(STq), the average within and among population genetic variance-covariance matrices, G(W) and G(B), can be used as an additional test of the null expectation of neutral divergence, and allows for an investigation of whether natural populations have diverged along major or minor axes of genetic variance.
Evolution 07/2008; 62(6):1437-49. · 5.15 Impact Factor
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ABSTRACT: Many species engage in polyandry, resulting in the potential for sexual selection to continue post-copulation through sperm competition and/or cryptic female choice. The relative importance of pre- vs. post-copulatory processes remains unknown for most species despite this information being fundamental for understanding the evolutionary consequences of sexual selection. The Australian fruit fly Drosophila serrata has become a prominent model system for studying precopulatory sexual selection, such as mating preferences and their influence on the evolution of sexually selected traits. Here, we investigated polyandry and the potential for post-copulatory sexual selection in this species using indirect paternity analysis. We genotyped 21 wild-caught and 19 laboratory-reared mothers and their offspring (a total of 787 flies) at six microsatellite loci and found extensive polyandry, with all broods surveyed having at least two sires. Female remating rates were higher than in other Drosophila surveyed to date and no significant differences were found between laboratory and field populations. Additionally, we found evidence for biased sperm usage in several broods of D. serrata. Paternity skew occurred more frequently in broods from the field population than the laboratory one, suggesting differences between the two environments in the level of post-copulatory sexual selection. Our data suggest that D. serrata represents a promising system for studying the interaction between pre- and post-copulatory sexual selection in driving the evolution of sexually selected phenotypes.
Molecular Ecology 04/2008; 17(6):1589-96. · 5.52 Impact Factor
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ABSTRACT: Despite a dramatic increase in empirical estimates of phenotypic selection over the past two decades, we remain remarkably ignorant about variation in the multivariate fitness surfaces that shape the adaptive landscape. We develop a novel approach for quantifying patterns of spatial and/or temporal variation in multivariate selection that directly compares vectors of linear selection gradients (beta) and matrices of nonlinear selection gradients (gamma) that describe the multivariate fitness surface in each population. We apply this approach to estimates of sexual selection on a suite of cuticular hydrocarbons (CHCs) in males and females from nine geographic populations of Drosophila serrata. In males, variation in linear sexual selection was associated with the presence of the related species Drosophila birchii, suggesting that female mate preferences for male CHCs differ between sympatry and allopatry. This is consistent with previous experimental results suggesting that reproductive character displacement of male CHCs has resulted from selection caused by the presence of D. birchii. No significant associations were found for nonlinear sexual selection in males. In females, large-scale variation in both linear and nonlinear sexual selection was negatively associated with assumed-neutral population genetic structure, suggesting a key role for chance events in male mate preference divergence.
The American Naturalist 02/2008; 171(4):443-54. · 4.72 Impact Factor
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ABSTRACT: The evolution of sexual dimorphism involves an interaction between sex-specific selection and a breakdown of genetic constraints that arise because the two sexes share a genome. We examined genetic constraints and the effect of sex-specific selection on a suite of sexually dimorphic display traits in Drosophila serrata. Sexual dimorphism varied among nine natural populations covering a substantial portion of the species range. Quantitative genetic analyses showed that intersexual genetic correlations were high because of autosomal genetic variance but that the inclusion of X-linked effects reduced genetic correlations substantially, indicating that sex linkage may be an important mechanism by which intersexual genetic constraints are reduced in this species. We then explored the potential for both natural and sexual selection to influence these traits, using a 12-generation laboratory experiment in which we altered the opportunities for each process as flies adapted to a novel environment. Sexual dimorphism evolved, with natural selection reducing sexual dimorphism, whereas sexual selection tended to increase it overall. To this extent, our results are consistent with the hypothesis that sexual selection favors evolutionary divergence of the sexes. However, sex-specific responses to natural and sexual selection contrasted with the classic model because sexual selection affected females rather than males.
The American Naturalist 02/2008; 171(1):22-34. · 4.72 Impact Factor
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ABSTRACT: Cuticular hydrocarbons (CHCs) act as contact pheromones in Drosophila melanogaster and are an important component of several ecological traits. Segregating genetic variation in the expression of CHCs at the population level in D. melanogaster is likely to be important for mate choice and climatic adaptation; however, this variation has never been characterized. Using a panel of recombinant inbred lines (RILs) derived from a natural population, we found significant between-line variation for nearly all CHCs in both sexes. We identified 25 QTL in females and 15 QTL in males that pleiotropically influence CHC expression. There was no evidence of colocalization of QTL for homologous traits across the sexes, indicating that sexual dimorphism and low intersex genetic correlations between homologous CHCs are a consequence of largely independent genetic control. This is consistent with a pattern of divergent sexual and natural selection between the sexes.
Genetics 04/2007; 175(3):1465-77. · 4.01 Impact Factor
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ABSTRACT: The use of transcriptional profiles for predicting mosquito age is a novel solution for the longstanding problem of determining the age of field-caught mosquitoes. Female mosquito age is of central importance to the transmission of a range of human pathogens. The transcriptional age-grading protocol we present here was developed in Aedes aegypti, principally as a research tool. Age predictions are made on the basis of transcriptional data collected from mosquitoes of known age. The abundance of eight candidate gene transcripts is quantified relative to a reference gene using quantitative reverse transcriptase-PCR (RT-PCR). Normalized gene expression (GE) measures are analyzed using canonical redundancy analysis to obtain a multivariate predictor of mosquito age. The relationship between the first redundancy variate and known age is used as the calibration model. Normalized GE measures are quantified for wild-caught mosquitoes, and ages are then predicted using this calibration model. Rearing of mosquitoes to specific ages for calibration data can take up to 40 d. Molecular analysis of transcript abundance, and subsequent age predictions, should take approximately 3-5 d for 100 individuals.
Nature Protocol 02/2007; 2(11):2796-806. · 8.36 Impact Factor
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ABSTRACT: The net effect of sexual selection on nonsexual fitness is controversial. On one side, elaborate display traits and preferences for them can be costly, reducing the nonsexual fitness of individuals possessing them, as well as their offspring. In contrast, sexual selection may reinforce nonsexual fitness if an individual's attractiveness and quality are genetically correlated. According to recent models, such good-genes mate choice should increase both the extent and rate of adaptation. We evolved 12 replicate populations of Drosophila serrata in a powerful two-way factorial experimental design to test the separate and combined contributions of natural and sexual selection to adaptation to a novel larval food resource. Populations evolving in the presence of natural selection had significantly higher mean nonsexual fitness when measured over three generations (13-15) during the course of experimental evolution (16-23% increase). The effect of natural selection was even more substantial when measured in a standardized, monogamous mating environment at the end of the experiment (generation 16; 52% increase). In contrast, and despite strong sexual selection on display traits, there was no evidence from any of the four replicate fitness measures that sexual selection promoted adaptation. In addition, a comparison of fitness measures conducted under different mating environments demonstrated a significant direct cost of sexual selection to females, likely arising from some form of male-induced harm. Indirect benefits of sexual selection in promoting adaptation to this novel resource environment therefore appear to be absent in this species, despite prior evidence suggesting the operation of good-genes mate choice in their ancestral environment. How novel environments affect the operation of good-genes mate choice is a fundamental question for future sexual selection research.
Evolution 12/2006; 60(11):2218-25. · 5.15 Impact Factor
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ABSTRACT: Age is a critical determinant of an adult female mosquito's ability to transmit a range of human pathogens. Despite its central importance, relatively few methods exist with which to accurately determine chronological age of field-caught mosquitoes. This fact is a major constraint on our ability to fully understand the relative importance of vector longevity to disease transmission in different ecological contexts. It also limits our ability to evaluate novel disease control strategies that specifically target mosquito longevity. We report the development of a transcriptional profiling approach to determine age of adult female Aedes aegypti under field conditions. We demonstrate that this approach surpasses current cuticular hydrocarbon methods for both accuracy of predicted age as well as the upper limits at which age can be reliably predicted. The method is based on genes that display age-dependent expression in a range of dipteran insects and, as such, is likely to be broadly applicable to other disease vectors.
Proceedings of the National Academy of Sciences 12/2006; 103(48):18060-5. · 9.68 Impact Factor
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ABSTRACT: The genetic analysis of mate choice is fraught with difficulties. Males produce complex signals and displays that can consist of a combination of acoustic, visual, chemical and behavioural phenotypes. Furthermore, female preferences for these male traits are notoriously difficult to quantify. During mate choice, genes not only affect the phenotypes of the individual they are in, but can influence the expression of traits in other individuals. How can genetic analyses be conducted to encompass this complexity? Tighter integration of classical quantitative genetic approaches with modern genomic technologies promises to advance our understanding of the complex genetic basis of mate choice.
Nature Reviews Genetics 10/2006; 7(9):681-92. · 38.08 Impact Factor
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ABSTRACT: Recent studies have demonstrated male mate choice for female ornaments in species without sex-role reversal. Despite these empirical findings, little is known about the adaptive dynamics of female signalling, in particular the evolution of male mating preferences. The evolution of traits that signal mate quality is more complex in females than in males because females usually provide the bulk of resources for the developing offspring. Here, we investigate the evolution of male mating preferences using a mathematical model which: (i) specifically accounts for the fact that females must trade-off resources invested in ornaments with reproduction; and (ii) allows male mating preferences to evolve a non-directional shape. The optimal adaptive strategy for males is to develop stabilizing mating preferences for female display traits to avoid females that either invests too many or too few resources in ornamentation. However, the evolutionary stability of this prediction is dependent upon the level of error made by females when allocating resources to either signal or fecundity.
Ecology Letters 03/2006; 9(2):179-84. · 17.56 Impact Factor
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ABSTRACT: Mating preferences are common in natural populations, and their divergence among populations is considered an important source of reproductive isolation during speciation. Although mechanisms for the divergence of mating preferences have received substantial theoretical treatment, complementary experimental tests are lacking. We conducted a laboratory evolution experiment, using the fruit fly Drosophila serrata, to explore the role of divergent selection between environments in the evolution of female mating preferences. Replicate populations of D. serrata were derived from a common ancestor and propagated in one of three resource environments: two novel environments and the ancestral laboratory environment. Adaptation to both novel environments involved changes in cuticular hydrocarbons, traits that predict mating success in these populations. Furthermore, female mating preferences for these cuticular hydrocarbons also diverged among populations. A component of this divergence occurred among treatment environments, accounting for at least 17.4% of the among-population divergence in linear mating preferences and 17.2% of the among-population divergence in nonlinear mating preferences. The divergence of mating preferences in correlation with environment is consistent with the classic by-product model of speciation in which premating isolation evolves as a side effect of divergent selection adapting populations to their different environments.
PLoS Biology 12/2005; 3(11):e368. · 11.45 Impact Factor
