Does artificial selection on diapause incidence cause correlational changes in other life‐history traits? Case study in a spider mite population

Theoretical studies suggest that the timing of entering hibernation by arthropods has large effects on long-term fitness, incurring strong selection pressure on diapause attributes every year. On the other hand, diapause attributes are often genetically correlated with other important life-history traits such as fecundity or development time. To understand the evolutionary process of life cycle formation, there is a need to investigate not only diapause attributes themselves but also their genetic association with other life-history traits. The Kanzawa spider mite, Tetranychus kanzawai Kishida (Acari: Tetranychidae), is a small herbivore that lives on the undersurface of host plant leaves. This mite has been investigated for the mode of inheritance of diapause attributes, but scarcely for genetic correlations with other life-history traits. Here, I investigated whether diapause proneness, measured as the proportion of diapausing females under short-day conditions, is genetically correlated with fecundity or development time under long-day conditions using artificial selection experiments. Diapause incidence responded to the selection for both increasing and decreasing directions, suggesting that high genetic variance in diapause proneness is maintained in the study population. However, the change in proportion of diapausing females during the selection period was not associated with responses in fecundity or development time. These results suggest that diapause proneness and other life-history traits have different genetic backgrounds, and thus diapause proneness may freely evolve without being constrained by changes in other life-history traits.     

Niche construction through germination cueing: life-history responses to timing of germination in Arabidopsis thaliana

Germination responses to seasonal conditions determine the environment experienced by postgermination life stages, and this ability has potential consequences for the evolution of plant life histories. Using recombinant inbred lines of Arabidopsis thaliana, we tested whether life-history characters exhibited plasticity to germination timing, whether germination timing influenced the strength and mode of natural selection on life-history traits, and whether germination timing influenced the expression of genetic variation for life-history traits. Adult life-history traits exhibited strong plasticity to season of germination, and season of germination significantly altered the strength, mode, and even direction of selection on life-history traits under some conditions. None of the average plastic responses to season of germination or season of dispersal were adaptive, although some genotypes within our sample did exhibit adaptive responses. Thus, recombination between inbred lineages created some novel adaptive genotypes with improved responses to the seasonal timing of germination under some, but not all, conditions. Genetically based variation in germination time tended to augment genetic variances of adult life-history traits, but it did not increase the heritabilities because it also increased environmentally induced variance. Under some conditions, plasticity of life-history traits in response to genetically variable germination timing actually obscured genetic variation for those traits. Therefore, the evolution of germination responses can influence the evolution of life histories in a general manner by altering natural selection on life-history traits and the genetic variation of these traits.     

THE MAINTENANCE OF GENETIC VARIATION FOR OVIPOSITION RATE IN TWO‐SPOTTED SPIDER MITES: INFERENCES FROM ARTIFICIAL SELECTION

Despite the directional selection acting on life‐history traits, substantial amounts of standing variation for these traits have frequently been found. This variation may result from balancing selection (e.g., through genetic trade‐offs) or from mutation‐selection balance. These mechanisms affect allele frequencies in different ways: Under balancing selection alleles are maintained at intermediate frequencies, whereas under mutation‐selection balance variation is generated by deleterious mutations and removed by directional selection, which leads to asymmetry in the distribution of allele frequencies. To investigate the importance of these two mechanisms in maintaining heritable variation in oviposition rate of the two‐spotted spider mite, we analyzed the response to artificial selection. In three replicate experiments, we selected for higher and lower oviposition rate, compared to control lines. A response to selection only occurred in the downward direction. Selection for lower oviposition rate did not lead to an increase in any other component of fitness, but led to a decline in female juvenile survival. The results suggest standing variation for oviposition rate in this population consists largely of deleterious alleles, as in a mutation‐selection balance. Consequently, the standing variation for this trait does not appear to be indicative of its adaptive potential.     

Genetic analysis of life-history constraint and evolution in a wild ungulate population

Trade-offs among life-history traits are central to evolutionary theory. In quantitative genetic terms, trade-offs may be manifested as negative genetic covariances relative to the direction of selection on phenotypic traits. Although the expression and selection of ecologically important phenotypic variation are fundamentally multivariate phenomena, the in situ quantification of genetic covariances is challenging. Even for life-history traits, where well-developed theory exists with which to relate phenotypic variation to fitness variation, little evidence exists from in situ studies that negative genetic covariances are an important aspect of the genetic architecture of life-history traits. In fact, the majority of reported estimates of genetic covariances among life-history traits are positive. Here we apply theory of the genetics and selection of life histories in organisms with complex life cycles to provide a framework for quantifying the contribution of multivariate genetically based relationships among traits to evolutionary constraint. We use a Bayesian framework to link pedigree-based inference of the genetic basis of variation in life-history traits to evolutionary demography theory regarding how life histories are selected. Our results suggest that genetic covariances may be acting to constrain the evolution of female life-history traits in a wild population of red deer Cervus elaphus: genetic covariances are estimated to reduce the rate of adaptation by about 40%, relative to predicted evolutionary change in the absence of genetic covariances. Furthermore, multivariate phenotypic (rather than genetic) relationships among female life-history traits do not reveal this constraint.     

Consequences of hierarchical allocation for the evolution of life-history traits

Resource allocation within individuals may often be hierarchical, and this may have important effects on genetic correlations and on trait evolution. For example, organisms may divide energy between reproduction and somatic growth and then subdivide reproductive resources. Genetic variation in allocation to pathways early in such hierarchies (e.g., reproduction) can cause positive genetic correlations between traits that trade off (e.g., offspring size and number) because some individuals invest more resources in reproduction than others. We used quantitative-genetic models to explore the evolutionary implications of allocation hierarchies. Our results showed that when variation in allocation early in the hierarchy exceeds subsequent variation in allocation, genetic covariances and initial responses to selection do not reflect trade-offs occurring at later levels in the hierarchy. This general pattern was evident for many starting allocations and optima and for whether traits contributed multiplicatively or additively to fitness. Finally, artificial selection on a single trait revealed masked trade-offs when variation in early allocation was comparable to subsequent variation in allocation. This result confirms artificial selection as a powerful, but not foolproof, method of detecting trade-offs. Thus, allocation hierarchies can profoundly affect life-history evolution by causing traits to evolve in the opposite direction to that predicted by trade-offs.     

Bidirectional selection for female propensity to remate in the bean beetle, <Emphasis Type="Italic">Callosobruchus chinensis</Emphasis>

The evolution of female multiple mating, or polyandry, is difficult to comprehend and thus has been the subject of a large number of studies. However, there is only a little evidence for genetic variation in polyandry, although the evolution of a trait via selection requires genetic variation that enables the trait to respond to selection. We carried out artificial selection for increased and decreased female propensity to remate as a measure of polyandry to investigate whether this trait has a genetic component that can respond to selection in the adzuki bean beetle, Callosobruchus chinensis. Artificial selection produced responses in both directions and divergence between the selection lines in the female propensity to remate. Although the experimental design adopted in this study selected jointly for female receptivity to remating, which is a trait of females, and male ability to inhibit female remating—both of which are associated with female propensity to remate—the observed response to selection was attributable only to the female receptivity to remating. This study indicates that the female receptivity to remating has significant additive genetic variation and can evolve according to whether remating is advantageous or disadvantageous to females in C. chinensis.     

THE EVOLUTIONARY GENETICS OF MALE LIFE-HISTORY CHARACTERS IN DROSOPHILA MELANOGASTER

Alternative models of the maintenance of genetic variability, theories of life-history evolution, and theories of sexual selection and mate choice can be tested by measuring additive and nonadditive genetic variances of components of fitness. A quantitative genetic breeding design was used to produce estimates of genetic variances for male life-history traits in Drosophila melanogaster. Additive genetic covariances and correlations between traits were also estimated. Flies from a large, outbred, laboratory population were assayed for age-specific competitive mating ability, age-specific survivorship, body mass, and fertility. Variance-component analysis then allowed the decomposition of phenotypic variation into components associated with additive genetic, nonadditive genetic, and environmental variability. A comparison of dominance and additive components of genetic variation provides little support for an important role for balancing selection in maintaining genetic variance in this suite of traits. The results provide support for the mutation-accumulation theory, but not the antagonistic-pleiotropy theory of senescence. No evidence is found for the positive genetic correlations between mating success and offspring quality or quantity that are predicted by “good genes” models of sexual selection. Additive genetic coefficients of variation for life-history characters are larger than those for body weight. Finally, this set of male life-history characters exhibits a very low correspondence between estimates of genetic and phenotypic correlations.     

On the evolution of clonal plant life histories

Clonal plant life histories are special in at least four respects: (1) Clonal plants can also reproduce vegetatively, (2) vegetative reproduction can be realised with short or long spacers, (3) and it may allow to plastically place vegetative offspring in benign patches. (4) Moreover, ramets of clonal plants may remain physically and physiologically integrated. Because of the apparent utility of such traits and because ecological patterns of distribution of clonal and non-clonal plants differ, adaptation is a tempting explanation of observed clonal life-history variation. However, adaptive evolution requires (1) heritable genetic variation and (2) a trait effect on fitness, and (3) it may be constrained if other evolutionary forces are overriding selection or by constraints, costs and trade-offs. (1) The few studies undertaken so far reported broad-sense heritability for clonal traits. Variation in selectively neutral genetic markers appears as pronounced in populations of clonal as non-clonal plants. However, neutral markers may not reflect heritable variation of life-history traits. Moreover, clonal plants may have been sampled at larger spatial scales. Empirical information on the contribution of somatic mutations to heritable variation is lacking. (2) Clonal life-history traits were found to affect fitness. However, much of this evidence stems from artificial rather than natural environments. (3) The relative importance of gene flow, inbreeding, and genetic drift, compared with selection, in the evolution of clonal life histories is hardly explored. Benefits of clonal life-history traits were frequently studied and found. However, there is also evidence for constraints, trade-offs, and costs. In conclusion, though it is very likely, that clonal life-history traits are adaptive, it is neither clear to which degree this is the case, nor which clonal life-history traits constitute adaptations to which environmental factors. Moreover, evolutionary interactions among clonal life-history traits and between clonal and non-clonal ones, such as the mating system, are not well explored. There remains much interesting work to be done in this field – which will be particularly interesting if it is done in the field.     

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

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

Testing the role of phenotypic plasticity for local adaptation: growth and development in time-constrained Rana temporaria populations

Phenotypic plasticity can be important for local adaptation, because it enables individuals to survive in a novel environment until genetic changes have been accumulated by genetic accommodation. By analysing the relationship between development rate and growth rate, it can be determined whether plasticity in life-history traits is caused by changed physiology or behaviour. We extended this to examine whether plasticity had been aiding local adaptation, by investigating whether the plastic response had been fixed in locally adapted populations. Tadpoles from island populations of Rana temporaria, locally adapted to different pool-drying regimes, were monitored in a common garden. Individual differences in development rate were caused by different foraging efficiency. However, developmental plasticity was physiologically mediated by trading off growth against development rate. Surprisingly, plasticity has not aided local adaptation to time-stressed environments, because local adaptation was not caused by genetic assimilation but on selection on the standing genetic variation in development time.     

Evidence for strong intralocus sexual conflict in the Indian meal moth, Plodia interpunctella

Males and females share a genome and express many shared phenotypic traits, which are often selected in opposite directions. This generates intralocus sexual conflict that may constrain trait evolution by preventing the sexes from reaching their optimal phenotype. Furthermore, if present across multiple loci, intralocus sexual conflict can result in a gender load that may diminish the benefits of sexual selection and help maintain genetic variation for fitness. Despite the importance of intralocus sexual conflict, surprisingly few empirical studies conclusively demonstrate its operation. We show that the pattern of multivariate selection acting on three sexually dimorphic life-history traits (development time, body size, and longevity) in the Indian meal moth, Plodia interpunctella, is opposing for the sexes. Moreover, we combined our estimates of selection with the additive genetic variance-covariance matrix (G) to predict the evolutionary response of the life-history traits in the sexes and showed that the angle between the vector of responses and the vector of sexually antagonistic selection was almost orthogonal at 84.70°. Thus, G biases the predicted response of life-history traits in the sexes away from the direction of sexually antagonistic selection, confirming the presence of strong intralocus sexual conflict in this species. Despite this, sexual dimorphism has evolved in all of the life-history traits examined suggesting that mechanism(s) have evolved to resolve this conflict and allow the sexes to reach their life-history optima. We argue that intralocus sexual conflict is likely to play an important role in the evolution of divergent life-history strategies between the sexes in this species.     

Heritability and artificial selection on ambulatory dispersal distance in Tetranychus urticae: effects of density and maternal effects

Dispersal distance is understudied although the evolution of dispersal distance affects the distribution of genetic diversity through space. Using the two-spotted spider mite, Tetranychus urticae, we tested the conditions under which dispersal distance could evolve. To this aim, we performed artificial selection based on dispersal distance by choosing 40 individuals (out of 150) that settled furthest from the home patch (high dispersal, HDIS) and 40 individuals that remained close to the home patch (low dispersal, LDIS) with three replicates per treatment. We did not observe a response to selection nor a difference between treatments in life-history traits (fecundity, survival, longevity, and sex-ratio) after ten generations of selection. However, we show that heritability for dispersal distance depends on density. Heritability for dispersal distance was low and non-significant when using the same density as the artificial selection experiments while heritability becomes significant at a lower density. Furthermore, we show that maternal effects may have influenced the dispersal behaviour of the mites. Our results suggest primarily that selection did not work because high density and maternal effects induced phenotypic plasticity for dispersal distance. Density and maternal effects may affect the evolution of dispersal distance and should be incorporated into future theoretical and empirical studies.     

Artificial evolution of life history and behavior

We present an individual-based model that uses artificial evolution to predict fit behavior and life-history traits on the basis of environmental data and organism physiology. Our main purpose is to investigate whether artificial evolution is a suitable tool for studying life history and behavior of real biological organisms. The evolutionary adaptation is founded on a genetic algorithm that searches for improved solutions to the traits under scrutiny. From the genetic algorithm's "genetic code," behavior is determined using an artificial neural network. The marine planktivorous fish Müller's pearlside (Maurolicus muelleri) is used as the model organism because of the broad knowledge of its behavior and life history, by which the model's performance is evaluated. The model adapts three traits: habitat choice, energy allocation, and spawning strategy. We present one simulation with, and one without, stochastic juvenile survival. Spawning pattern, longevity, and energy allocation are the life-history traits most affected by stochastic juvenile survival. Predicted behavior is in good agreement with field observations and with previous modeling results, validating the usefulness of the presented model in particular and artificial evolution in ecological modeling in general. The advantages, possibilities, and limitations of this modeling approach are further discussed.     

Adaptation in a spider mite population after long-term evolution on a single host plant

Evolution in a single environment is expected to erode genetic variability, thereby precluding adaptation to novel environments. To test this, a large population of spider mites kept on cucumber for approximately 300 generations was used to establish populations on novel host plants (tomato or pepper), and changes in traits associated to adaptation were measured after 15 generations. Using a half-sib design, we investigated whether trait changes were related to genetic variation in the base population. Juvenile survival and fecundity exhibited genetic variation and increased in experimental populations on novel hosts. Conversely, no variation was detected for host choice and developmental time and these traits did not evolve. Longevity remained unchanged on novel hosts despite the presence of genetic variation, suggesting weak selection for this trait. Hence, patterns of evolutionary changes generally matched those of genetic variation, and changes in some traits were not hindered by long-term evolution in a constant environment.     

SEX RATIO VARIATION IN A PARASITIC WASP II. DIALLEL CROSS

Sex ratio has been studied from many theoretical and empirical perspectives, but a general assumption in sex ratio research is that changes in sex ratio occur because of selection on sex ratio itself. I carried out a quantitative genetic experiment—a diallel cross among three strains—on a parasitic wasp, Muscidifurax raptor (Hymenoptera: Pteromalidae), to measure genetic variation for sex ratio. I also tested whether sex ratio may change as a consequence of selection on other life-history traits by estimating genetic covariances between sex ratio, fecundity, longevity, and development time. Most of the variation among strains could be accounted for by a maternal effect, likely caused by a microsporidian parasite that was transmitted through the West Germany (WG) strain. Genetic variation was small by comparison, but almost all traits were affected by dominance. The only significant additive genetic effect was for fecundity early in life. Upon crossing, all traits displayed heterosis: more female-biased sex ratio, greater fecundity, longer life, and faster development time. All life-history traits were correlated phenotypically, but the correlations were mainly the result of decreased performance in crosses with the WG strain that carried the microsporidian parasite. Dominance genetic correlations were also found between sex ratio, fecundity, and longevity. How the correlation between sex ratio and other life-history traits would affect sex ratio evolution depends upon the frequencies of sex-ratio genotypes within a population as well as the signs of the correlations, because sex ratio is under frequency-dependent selection whereas other traits are generally under directional selection. Although the results from crosses among laboratory populations should be approached with caution, the inbreeding depression (the difference between inbred and outcrossed progeny) found in M. raptor implies that the evolution of a female-biased sex ratio could be affected by selection for inbreeding avoidance.     

Realized correlated responses to artificial selection on pre-adult life-history traits in a butterfly

We use artificial selection experiments targeted on egg size, development time or pupal mass within a single butterfly population followed by a common-garden experiment to explore the interactions among these life-history traits. Relationships were predicted to be negative between egg size and development time, but to be positive between development time and body size and between egg size and body size. Correlated responses to selection were in part inconsistent with these predictions. Although there was evidence for a positive genetic correlation between egg and body size, there was no support for genetic correlations between larval development time and either egg size or pupal mass. Phenotypic correlations among the three target traits of selection gave comparable results for the relationships between egg mass and development time (no association) as well as between egg mass and pupal mass (positive association), but not for the relation between development time and pupal mass (negative phenotypic correlation). In summary, correlated responses to selection as well as phenotypic correlations were rather unpredictable. The impact of variation in acquisition and allocation of energy as well as of the benign conditions used deserve further investigation.     

The evolution of alternative developmental pathways: footprints of selection on life-history traits in a butterfly

Developmental pathways may evolve to optimize alternative phenotypes across environments. However, the maintenance of such adaptive plasticity under relaxed selection has received little study. We compare the expression of life-history traits across two developmental pathways in two populations of the butterfly Pararge aegeria where both populations express a diapause pathway but one never expresses direct development in nature. In the population with ongoing selection on both pathways, the difference between pathways in development time and growth rate was larger, whereas the difference in body size was smaller compared with the population experiencing relaxed selection on one pathway. This indicates that relaxed selection on the direct pathway has allowed life-history traits to drift towards values associated with lower fitness when following this pathway. Relaxed selection on direct development was also associated with a higher degree of genetic variation for protandry expressed as within-family sexual dimorphism in growth rate. Genetic correlations for larval growth rate across sexes and pathways were generally positive, with the notable exception of correlation estimates that involved directly developing males of the population that experienced relaxed selection on this pathway. We conclude that relaxed selection on one developmental pathway appears to have partly disrupted the developmental regulation of life-history trait expression. This in turn suggests that ongoing selection may be responsible for maintaining adaptive developmental regulation along alternative developmental pathways in these populations.     

Variation in tolerance to drought among Scandinavian populations of <Emphasis Type="Italic">Arabidopsis lyrata</Emphasis>

The ability to cope with water limitation influences plant distributions, and several plant traits have been interpreted as adaptations to drought stress. In Scandinavia, the perennial herb Arabidopsis lyrata occurs in open habitats that differ widely in climate and water availability in summer, suggesting differential selection on drought-related traits. We conducted two greenhouse experiments to examine differentiation in drought response traits among six Scandinavian populations, and to determine whether leaf trichomes confer protection against drought. We quantified tolerance to drought as fitness (survival and biomass of survivors) when exposed to drought relative to fitness under non-drought conditions. Two Swedish populations from shores along the Bothnian Bay had higher tolerance to drought than four riverbed populations from Norway. Under conditions of drought, the shore populations experienced less leaf damage compared to the riverbed populations, and their survival and biomass were less reduced relative to non-drought conditions. Across populations, tolerance to drought was positively related to leaf mass per area and negatively related to flowering propensity and proportion roots, but not related to plant size at the initiation of the drought treatment. In populations polymorphic for trichome production, trichome-producing plants were more tolerant to drought than glabrous plants. The results suggest that both leaf morphology and life-history traits contribute to differential drought response in natural populations of A. lyrata, and that this system offers excellent opportunities for examining the adaptive value and genetic basis of drought-related traits.     

Response of a complex foraging phenotype to artificial selection on its component traits

In nature, where predators must often track dynamic and dispersed prey populations, predator consumption rate, conversion efficiency, dispersal, and prey finding are likely to be important links between foraging and predator–prey population dynamics. Small differences in predator foraging caused by variation in any of the abovementioned traits might lead to significant differences in predator success as well as population dynamics. We used artificial selection to create lines of the predatory mite, Phytoseiulus persimilis in order to determine the potential for or constraints on the evolution of predator foraging behaviors. All four foraging traits demonstrated considerable phenotypic variation. They also exhibited significant realized heritabilities after artificial selection, except that prey finding did not respond to downward selection. Lines that responded to selection did so rapidly, and high-consumption, high-conversion efficiency, and high- and low-dispersal were stable for at least four generations after artificial selection was relaxed. There were some indirect responses to selection among the foraging traits. For example, there was positive correlation between consumption and dispersal. However, none of the correlated responses were of the magnitude of the direct responses we measured on the same trait. We also observed some correlations between foraging traits and life-history traits such as low-consumption and development time (negative), high-consumption and fecundity (positive), and high-conversion efficiency and fecundity (positive), but these were more likely to represent non-genetic constraints. Intrinsic rates of increase in low-consumption and low-conversion efficiency lines were lower than in their respective high lines and the unselected control, whereas rates of increase in dispersal and olfactory response lines did not differ from the unselected control. Thus, traits that make up foraging share partially overlapping genetic architectures with highly heritable phenotypic components, suggesting that each foraging trait will be able to respond rapidly to changes in the density and distribution of resources.     

Artificial selection reveals heritable variation for developmental instability

Fluctuating (nondirectional) asymmetry (FA) of bilaterally paired structures on a symmetrical organism is commonly used to assay the developmental instability (DI) caused by environmental or genetic factors. Although evidence for natural selection to reduce FA has been reported, evidence that FA (and by extension DI) is heritable is weak. We report the use of artificial selection to demonstrate heritable variation in the fluctuating asymmetry of interlandmark distances within the wing in an outbred population of Drosophila melanogaster. Our estimates for the heritability of FA range from 0% to 1% and result in estimates for the heritability of DI as large as 20%, comparable to values typical for life-history traits. These values indicate the existence of evolutionarily relevant genetic variation for DI and the effectiveness of selection for reduced FA suggests that natural selection has not fixed all the genetic variants that would improve developmental stability in these populations.