Natural selection and quantitative genetics of life-history traits in Western women: A twin study

Whether contemporary human populations are still evolving as a result of natural selection has been hotly debated. For natural selection to cause evolutionary change in a trait, variation in the trait must be correlated with fitness and be genetically heritable and there must be no genetic constraints to evolution. These conditions have rarely been tested in human populations. In this study, data from a large twin cohort were used to assess whether selection Will cause a change among women in contemporary Western population for three life-history traits: age at menarche, age at first reproduction, and age at menopause. We control for temporal variation in fecundity (the baby boom phenomenon) and differences between women in educational background and religious affiliation. University-educated women have 35% lower fitness than those with less than seven years education, and Roman Catholic women have about 20% higher fitness than those of other religions. Although these differences were significant, education and religion only accounted for 2% and 1% of variance in fitness, respectively. Using structural equation modeling, we reveal significant genetic influences for all three life-history traits, with heritability estimates of 0.50, 0.23, and 0.45, respectively. However, strong genetic covariation with reproductive fitness could only be demonstrated for age at first reproduction, with much weaker covariation for age at menopause and no significant covariation for age at menarche. Selection may, therefore, lead to the evolution of earlier age at first reproduction in this population. We also estimate substantial heritable variation in fitness itself, with approximately 39% of the variance attributable to additive genetic effects, the remainder consisting of unique environmental effects and small effects from education and religion. We discuss mechanisms that could be maintaining such a high heritability for fitness. Most likely is that selection is now acting on different traits from which it did in pre-industrial human populations.

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.

Interaction between natural and sexual selection during the evolution of mate recognition

The interaction between natural and sexual selection is central to many theories of how mate choice and reproductive isolation evolve, but their joint effect on the evolution of mate recognition has not, to my knowledge, been investigated in an evolutionary experiment. Natural and sexual selection were manipulated in interspecific hybrid populations of Drosophila to determine their effects on the evolution of a mate recognition system comprised of cuticular hydrocarbons (CHCs). The effect of natural selection in isolation indicated that CHCs were costly for males and females to produce. The effect of sexual selection in isolation indicated that females preferred males with a particular CHC composition. However, the interaction between natural and sexual selection had a greater effect on the evolution of the mate recognition system than either process in isolation. When natural and sexual selection were permitted to operate in combination, male CHCs became exaggerated to a greater extent than in the presence of sexual selection alone, and female CHCs evolved against the direction of natural selection. This experiment demonstrated that the interaction between natural and sexual selection is critical in determining the direction and magnitude of the evolutionary response of the mate recognition system.

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.

The roles of natural and sexual selection during adaptation to a novel environment

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.

Geographic variation and positive selection on M7 lysin, an acrosomal sperm protein in mussels (Mytilus spp.)

Successful fertilization in free-spawning marine organisms depends on the interactions between genes expressed on the surfaces of eggs and sperm. Positive selection frequently characterizes the molecular evolution of such genes, raising the possibility that some common deterministic process drives the evolution of gamete recognition genes and may even be important for understanding the evolution of prezygotic isolation and speciation in the marine realm. One hypothesis is that gamete recognition genes are subject to selection for prezygotic isolation, namely reinforcement. In a previous study, positive selection on the gene coding for the acrosomal sperm protein M7 lysin was demonstrated among allopatric populations of mussels in the Mytilus edulis species group (M. edulis, M. galloprovincialis, and M. trossulus). Here, we expand sampling to include M7 lysin haplotypes from populations where mussel species are sympatric and hybridize to determine whether there is a pattern of reproductive character displacement, which would be consistent with reinforcement driving selection on this gene. We do not detect a strong pattern of reproductive character displacement; there are no unique haplotypes in sympatry nor is there consistently greater population structure in comparisons involving sympatric populations. One distinct group of haplotypes, however, is strongly affected by natural selection and this group of haplotypes is found within M. galloprovincialis populations throughout the Northern Hemisphere concurrent with haplotypes common to M. galloprovincialis and M. edulis. We suggest that balancing selection, perhaps resulting from sexual conflicts between sperm and eggs, maintains old allelic diversity within M. galloprovincialis.

Life-history consequences of divergent selection on egg size in Drosophila melanogaster

Life histories are generally assumed to evolve via antagonistic pleiotropy (negative genetic correlations) among traits, and trade-offs between life-history traits are typically studied using either phenotypic manipulations or selection experiments. We investigated the trade-off between egg size and fecundity in Drosophila melanogaster by examining both the phenotypic and genetic relationships between these traits after artificial selection for large and small eggs, relative to female body size. Egg size responded strongly to selection in both directions, increasing in the large-egg selected lines and decreasing in the small-egg selected lines. Phenotypic correlations between egg size and fecundity in the large-egg selected lines were negative, but no relationship between these traits occurred in either the control or small-egg selected lines. There was no negative genetic correlation between egg size and fecundity. Total reproductive allocation decreased in the small-egg selected lines but did not increase in the large-egg lines. Our results have three implications. First, our selection procedure may have forced females selected for large eggs into a physiological trade-off not reflected in a negative genetic correlation between these traits. Second, the lack of a negative genetic correlation between egg size and number suggests that the phenotypic trade-off frequently observed between egg size and number in other organisms may not evolve over the short term via a direct genetic trade-off whereby increases in egg size are automatically accompanied by decreased fecundity. Finally, total reproductive allocation may not evolve independently of egg size as commonly assumed.

Microevolution in island forms: the roles of drift and directional selection in morphological divergence of a passerine bird

Theory predicts that in small isolated populations random genetic drift can lead to phenotypic divergence; however this prediction has rarely been tested quantitatively in natural populations. Here we utilize natural repeated island colonization events by members of the avian species complex, Zosterops lateralis, to assess whether or not genetic drift alone is an adequate explanation for the observed patterns of microevolutionary divergence in morphology. Morphological and molecular genetic characteristics of island and mainland populations are compared to test three predictions of drift theory: (1) that the pattern of morphological change is idiosyncratic to each island; (2) that there is concordance between morphological and neutral genetic shifts across island populations; and (3) for populations whose time of colonization is known, that the rate of morphological change is sufficiently slow to be accounted for solely by genetic drift. Our results are not consistent with these predictions. First, the direction of size shifts was consistently towards larger size, suggesting the action of a nonrandom process. Second, patterns of morphological divergence among recently colonized populations showed little concordance with divergence in neutral genetic characters. Third, rate tests of morphological change showed that effective population sizes were not small enough for random processes alone to account for the magnitude of microevolutionary change. Altogether, these three lines of evidence suggest that drift alone is not an adequate explanation of morphological differentiation in recently colonized island Zosterops and therefore we suggest that the observed microevolutionary changes are largely a result of directional natural selection.

Conspicuous males suffer higher predation risk: visual modelling and experimental evidence from lizards

Colour pattern variation is a striking and widespread phenomenon. Differential predation risk between individuals is often invoked to explain colour variation, but empirical support for this hypothesis is equivocal. We investigated differential conspicuousness and predation risk in two species of Australian rock dragons, Ctenophorus decresii and C. vadnappa. To humans, the coloration of males of these species varies between 'bright' and 'dull'. Visual modelling based on objective colour measurements and the spectral sensitivities of avian visual pigments showed that dragon colour variants are differentially conspicuous to the visual system of avian predators when viewed against the natural background. We conducted field experiments to test for differential predation risk, using plaster models of 'bright' and 'dull' males. 'Bright' models were attacked significantly more often than 'dull' models suggesting that differential conspicuousness translates to differential predation risk in the wild. We also examined the influence of natural geographical range on predation risk. Results from 22 localities suggest that predation rates vary according to whether predators are familiar with the prey species. This study is among the first to demonstrate both differential conspicuousness and differential predation risk in the wild using an experimental protocol. (C) 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.

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.

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.

Parallel evolution of sexual isolation in sticklebacks

Mechanisms of speciation are not well understood, despite decades of study. Recent work has focused on how natural and sexual selection cause sexual isolation. Here, we investigate the roles of divergent natural and sexual selection in the evolution of sexual isolation between sympatric species of threespine sticklebacks. We test the importance of morphological and behavioral traits in conferring sexual isolation and examine to what extent these traits have diverged in parallel between multiple, independently evolved species pairs. We use the patterns of evolution in ecological and mating traits to infer the likely nature of selection on sexual isolation. Strong parallel evolution implicates ecologically based divergent natural and/or sexual selection, whereas arbitrary directionality implicates nonecological sexual selection or drift. In multiple pairs we find that sexual isolation arises in the same way: assortative mating on body size and asymmetric isolation due to male nuptial color. Body size and color have diverged in a strongly parallel manner, similar to ecological traits. The data implicate ecologically based divergent natural and sexual selection as engines of speciation in this group.