Selection response in traits with maternal inheritance

Maternal inheritance is the non-Mendelian transmission of traits from mothers to their offspring. Despite its presence in virtually all organisms, acting through a variety of mechanisms, the evolutionary consequences of maternal inheritance are not well understood. Here we review and extend a model of the inheritance and evolution of multiple quantitative characters with complex pathways of maternal effects. Extensions of the earlier model include common family environmental effects not associated with maternal phenotype, sexual dimorphism, and paternal effects (non-Mendelian influence of the father on offspring traits). We find that, in contrast to simple Mendelian inheritance, maternal inheritance produces qualitatively different evolutionary dynamics for two reasons: (1) the response to selection on a set of characters depends not only on their additive genetic variances and covariances, but also on maternal characters that influence them, and (2) time lags in the response to selection create a form of evolutionary momentum. These results have important implications for evolution in natural populations and practical applications in the economic improvement of domesticated species. We derive selection indices that maximize either the economic improvement in a single generation of artificial selection or the asymptotic rate of improvement in long-term selection programmes, based on individual merit or a combination of individual and family merit. Numerical examples show that accounting for maternal inheritance can lead to considerable increases in the efficiency of artificial selection.     

Does experimental evolution produce better biological control agents? A critical review of the evidence

Biological control of crop pests is considered a good alternative or complement to the use of pesticides. However, legislation restricts the importation of natural enemies of pests. A potential way to circumvent this limitation is by using experimental evolution and/or artificial selection to improve native biological control agents. Here, we review studies that have used these methodologies and evaluate their success. Experimental evolution or artificial selection has been used on a wide range of traits, with most focusing on improving the performance of natural enemies in ecologically relevant environments, such as in the presence of pesticides or at different temperatures. Although most studies were poorly replicated, the selected traits generally improved following the selection process. However, correlated responses (often in the form of trade‐offs) with other traits of interest were common. We suggest that the selection procedure can be improved by increasing replication and performing experimental evolution under more semi‐natural environments, to ensure that the most useful traits are being selected.     

The evolution of the worldwide leaf economics spectrum

The worldwide leaf economic spectrum (WLES) is a strikingly consistent pattern of correlations among leaf traits. Although the WLES effectively summarizes variation in plant ecological strategies, little is known about its evolution. We reviewed estimates of natural selection and genetic variation for leaf traits to test whether the evolution of the WLES was limited by selection against unfit trait combinations or by genetic constraints. There was significant selection for leaf traits on both ends of the WLES spectrum, as well as significant genetic variation for these traits. In addition, genetic correlations between WLES traits were variable in strength and direction. These data suggest that genetic constraints have had a smaller role than selection in the evolution of the WLES.     

A behavioral perspective on fishing-induced evolution

The potential for excessive and/or selective fishing to act as an evolutionary force has been emphasized recently. However, most studies have focused on evolution of life-history traits in response to size-selective harvesting. Here we draw attention to fishing-induced evolution of behavioral and underlying physiological traits. We contend that fishing-induced selection directly acting on behavioral rather than on life-history traits per se can be expected in all fisheries that operate with passive gears such as trapping, angling and gill-netting. Recent artificial selection experiments in the nest-guarding largemouth bass Micropterus salmoides suggest that fishing-induced evolution of behavioral traits that reduce exposure to fishing gear might be maladaptive, potentially reducing natural recruitment. To improve understanding and management of fisheries-induced evolution, we encourage greater application of methods from behavioral ecology, physiological ecology and behavioral genetics.     

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.     

Economic weights of maternal and direct traits of pigs calculated by applying gene flow methods

Multiple trait selection indexes in pig breeding programmes should take into account the population structure and time delay between parent selection and expressions of traits in all production levels next to the trait impacts on economic efficiency of production systems. Gene flow procedures could be used for the correct evaluation of maternal and direct traits of pig breeds involved in breeding or crossbreeding systems. Therefore, the aim of this study was to expand a previously developed bioeconomic model and computer program to calculate the marginal economic values by including a gene flow procedure to calculate the economic weights for maternal and direct traits in pig breeds. The new program was then applied to the three-way crossbreeding system of the Czech National Programme for Pig Breeding. Using this program, the marginal economic values of traits for dam breeds Czech Large White in the dam position and Czech Landrace in the sire position, and for the sire breed Pietrain were weighted by the number of discounted gene expressions of selected parents of each breed summarised within all links of the crossbreeding system during the 8-year investment period. Economic weights calculated in this way were compared with the approximate economic weights calculated previously without a gene flow procedure. Taking into account the time delay between parent selection and trait expression (using discounting with half-year discount rates of 2% or 5%) and including more than one generation of parent progeny had little impact on the relative economic importance of maternal and direct traits of breeds involved in the evaluated three-way crossbreeding system. These results indicated that this gene-flow method could be foregone when estimating the relative economic weights of traits in pig crossbreeding systems applying artificial insemination at all production levels.     

Genetic independence of female signal form and male receiver design in the almond moth, Cadra cautella

Efficient signalling requires coordination of signal form and receiver design. To maintain signal function, parallel changes in signaller and receiver traits are required. Genetic correlation and co-evolution among signal and response traits have been proposed to preserve signal function (i.e. coordination) during the evolution of mate recognition systems. Empirical studies have provided support for both mechanisms; however, there is debate regarding the interpretation of some of these studies. Tests for a genetic correlation typically hybridize divergent signalling systems and look at hybrid signal form and receiver design, or impose artificial selection on signal form and look for an indirect response to selection in receiver design. Some of the hybridization studies did not achieve reassortment of genes from the parental types, whereas some of the artificial selection studies incorporated random mating in their designs. As a result of these limitations, the hybridization studies cannot discriminate between genetic correlation and co-evolution with primarily additive genetic effects underlying signal and response traits. Similarly, the artificial selection experiments cannot discriminate between genetic correlation because of linkage disequilibrium and co-evolution. This study examined the mating preferences of male almond moths, Cadra cautella, before and after female moths were artificially selected (using a design incorporating assortative mating) for novel pheromone blend ratios. Our results demonstrate the absence of a genetic correlation between signal and response traits in the almond moth.     

Internal and external constraints in the evolution of morphological allometries in a butterfly

Much diversity in animal morphology results from variation in the relative size of morphological traits. The scaling relationships, or allometries, that describe relative trait size can vary greatly in both intercept and slope among species or other animal groups. Yet within such groups, individuals typically exhibit low variation in relative trait size. This pattern of high intra- and low intergroup variation may result from natural selection for particular allometries, from developmental constraints restricting differential growth among traits, or both. Here we explore the relative roles of short-term developmental constraints and natural selection in the evolution of the intercept of the allometry between the forewing and hindwing of a butterfly. First, despite a strong genetic correlation between these two traits, we show that artificial selection perpendicular to the forewing-hindwing scaling relationship results in rapid evolution of the allometry intercept. This demonstrates an absence of developmental constraints limiting intercept evolution for this scaling relationship. Mating experiments in a natural environment revealed strong stabilizing selection favoring males with the wild-type allometry intercept over those with derived intercepts. Our results demonstrate that evolution of this component of the forewing-hindwing allometry is not limited by developmental constraints in the short term and that natural selection on allometry intercepts can be powerful.     

Natural selection hampers divergence of reproductive traits in a seed beetle

Speciation is thought to often result from indirect selection for reproductive isolation. This will occur when reproductive traits that cause reproductive isolation evolve (i) as a by‐product of natural selection on traits with which they are genetically correlated or (ii) as an indirect result of diversifying sexual selection. Here, we use experimental evolution to study the degree of divergent evolution of reproductive traits by manipulating the intensity of natural and sexual selection in replicated selection lines of seed beetles. Following 40 generations of selection, we assayed the degree of divergent evolution of reproductive traits between replicate selection lines experiencing the same selection regime. The evolution of reproductive traits was significantly divergent across selection lines within treatments. The evolution of reproductive traits was both slower and, more importantly, significantly less divergent among lines experiencing stronger directional natural selection. This suggests that reproductive traits did not evolve as an indirect by‐product of adaptation. We discuss several ways in which natural selection may hamper divergent evolution among allopatric populations.     

The evolution of trade-offs under directional and correlational selection

Using quantitative genetic theory, we develop predictions for the evolution of trade-offs in response to directional and correlational selection. We predict that directional selection favoring an increase in one trait in a trade-off will result in change in the intercept but not the slope of the trade-off function, with the mean value of the selected trait increasing and that of the correlated trait decreasing. Natural selection will generally favor an increase in some combination of trait values, which can be represented as directional selection on an index value. Such selection induces both directional and correlational selection on the component traits. Theory predicts that selection on an index value will also change the intercept but not the slope of the trade-off function but because of correlational selection, the direction of change in component traits may be in the same or opposite directions. We test these predictions using artificial selection on the well-established trade-off between fecundity and flight capability in the cricket, Gryllus firmus and compare the empirical results with a priori predictions made using genetic parameters from a separate half-sibling experiment. Our results support the predictions and illustrate the complexity of trade-off evolution when component traits are subject to both directional and correlational selection.     

Constraint and developmental dissociation of phenotypic integration in a genetically accommodated trait

SUMMARY The genetic accommodation of novel adaptive traits may be accompanied by the evolution of correlated traits that constrain adaptive evolution. Very little is known about the removal of maladaptive correlated traits. In the present study, body size was found to have evolved as a correlated trait during the artificial selection for a polyphenism and a monophenism, and the developmental basis underlying this correlated trait was investigated. The body size and coloration were found to be developmentally integrated by titers of the insect developmental hormone, juvenile hormone (JH). Attempts to uncouple the two traits resulted in the evolution of one of the body size determinants—the critical weight—but not the delay period whose evolution is constrained by JH titers. Thus, maladaptive correlated traits can be removed when multiple developmental modules exist, and the evolution of one or more of these modules is not constrained.     

Direct and correlated responses to artificial selection on sexual size dimorphism in the flour beetle, Tribolium castaneum

Sexual size dimorphism (SSD) is a conspicuous yet poorly understood pattern across many organisms. Although artificial selection is an important tool for studying the evolution of SSD, previous studies have applied selection to only a single sex or to both sexes in the same direction. In nature, however, SSD likely arises through sex-specific selection on body size. Here, we use Tribolium castaneum flour beetles to investigate the evolution of SSD by subjecting males and females to sexually antagonistic selection on body size (sexes selected in opposite directions). Additionally, we examined correlated responses to body size selection in larval growth rates and development time. After seven generations, SSD remained unchanged in all selected lines; this observed lack of response to short-term selection may be attributed to evolutionary constraints arising from between-sex body size correlations. Developmental traits showed complex correlated responses under different selection treatments. These results suggest that sex-specific larval development patterns may facilitate the evolution of SSD.     

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.     

Correlated evolution of life-history with size at maturity in Daphnia pulicaria: patterns within and between populations

Explaining the repeated evolution of similar sets of traits under similar environmental conditions is an important issue in evolutionary biology. The extreme alternative classes of explanations for correlated suites of traits are optimal adaptation and genetic constraint resulting from pleiotropy. Adaptive explanations presume that individual traits are free to evolve to their local optima and that convergent evolution represents particularly adaptive combinations of traits. Alternatively, if pleiotropy is strong and difficult to break, strong selection on one or a few particularly important characters would be expected to result in consistent correlated evolution of associated traits. If pleiotropy is common, we predict that the pattern of divergence among populations will consistently reflect the within-population genetic architecture. To test the idea that the multivariate life-history phenotype is largely a byproduct of strong selection on body size, we imposed divergent artificial selection on size at maturity upon two populations of the cladoceran Daphnia pulicaria, chosen on the basis of their extreme divergence in body size. Overall, the trajectory of divergence between the two natural populations did not differ from that predicted by the genetic architecture within each population. However, the pattern of correlated responses suggested the presence of strong pleiotropic constraints only for adult body size and not for other life-history traits. One trait, offspring size, appears to have evolved in a way different from that expected from the within-population genetic architecture and may be under stabilizing selection.     

Experimental studies of group selection: what do they tell us about group selection in nature?

The study of group selection has developed along two autonomous lines. One approach, which we refer to as the adaptationist school, seeks to understand the evolution of existing traits by examining plausible mechanisms for their evolution and persistence. The other approach, which we refer to as the genetic school, seeks to examine how currently acting artificial or natural selection changes traits within populations and focuses on current evolutionary change. The levels of selection debate lies mainly within the adaptationist school, whereas the experimental studies of group selection lie within the genetic school. Because of the very different traditions and goals of these two schools, the experimental studies of group selection have not had a major impact on the group selection debate. We review the experimental results of the genetic school in the context of the group selection controversy and address the following questions: Under what conditions is group selection effective? What is the genetic basis of a response to group selection? How common is group selection in nature?     

Divergence of a speciation trait through artificial selection: Insights into constraints,by-product effects and sexual isolation

Speciation and sexual isolation often occur when divergent female mating preferences target male secondary sexual traits. Despite the importance of such male signals, little is known about their evolvability and genetic linkage to other traits during speciation. To answer these questions, we imposed divergent artificial selection for 10 non-overlapping generations on the Inter-Pulse-Interval (IPI) of male courtship songs; which has been previously shown to be a major species recognition trait for females in the Drosophila athabasca species complex. Focusing on one of the species, Drosophila mahican (previously known as EA race), we examined IPI's: (1) rate of divergence, (2) response to selection in different directions, (3) genetic architecture of divergence and (4) by-product effects on other traits that have diverged in the species complex. We found rapid and consistent response for higher IPI but less response to lower IPI; implying asymmetrical constraints. Genetic divergence in IPI differed from natural species in X versus autosome contribution and in dominance, suggesting that evolution may take different paths. Finally, selection on IPI did not alter other components of male songs, or other ecological traits, and did not cause divergence in female preferences, as evidenced by lack of sexual isolation. This suggests that divergence of male courtship song IPI is unconstrained by genetic linkage with other traits in this system. This lack of linkage between male signals and other traits implies that female preferences or ecological selection can co-opt and mould specific male signals for species recognition free of genetic constraints from other traits.     

Response to selection on cold tolerance is constrained by inbreeding

The evolutionary potential of any given population is of fundamental importance for its longer term prospects. Modern land-use practices often result in small and isolated populations, increasing the risk of extinction through reduced genetic diversity as a consequence of inbreeding or drift. Such genetic erosion may also interfere with a population's evolutionary potential. In this study, we investigate the consequences of inbreeding on evolutionary potential (the ability to increase cold resistance) in a laboratory population of the tropical butterfly Bicyclus anynana. To explore constraints on evolution, we applied artificial selection to chill-coma recovery time, starting from three levels of inbreeding (outbred control, one or two full-sibling matings). Ten generations of selection produced highly divergent phenotypes, with the lines selected for increased cold tolerance showing about 28% shorter recovery times after cold exposure relative to unselected controls. Correlated responses to selection in 10 different life-history and stress-resistance traits were essentially absent. Inbred lines showed a weaker response to selection, indicating reduced evolutionary potential and thereby constraints on evolution. Inbreeding depression was still measurable in some traits after the course of selection. Traits more closely related to fitness showed a clear fitness rebound, suggesting a trait-specific impact of purging. Our findings have important implications for the longer term survival of small populations in fragmented landscapes.     

Using artificial selection to understand plastic plant phenotypes

The plasticity of any given trait, which has a genetic basisand which may or may not be adaptive, can intensify or attenuateevolved responses, and can itself evolve in response to selectiondepending on the scale of spatial or temporal heterogeneity.To investigate the complex function and evolution of plastictraits, an appealing yet challenging approach is assessing responsesto artificial selection. Here, I review how artificial selectionhas been employed to explore four botanical research themes:(1) relationships between plastic and evolved responses to multiplestresses, (2) integration of cellular, leaf-level, and whole-plantresponses to altered CO₂ concentrations, (3) photomorphogenicand photoperiodic development, both mediated by phytochromephotoreceptors, and (4) the evolution of the pest-induced myrosinase-glucosinolatesystem in cruciferous plants. These diverse topics are unifiednot only because they have been studied using artificial selectionexperiments, but also because they have considered variabilityin multiple traits affected by multiple factors in the externalenvironment. Limitations of such research include a dearth oflong-term studies; a surprising but often logistically necessaryomission of control or replicate lines; and numerous issuesrelating to assessing impacts of inbreeding and drift. In additionto discussing options for circumventing such limitations, Idraw attention to strategies for integrating the results ofartificial selection studies with progress in functional andevolutionary genomics.     

Mammalian sexual dimorphism

Sexual dimorphisms (SDs) have evolved in mammals to assure greater reproductive success for individuals, usually males. Secondary sexual characteristics (SSC) developed to further this objective, tending to be more pronounced in species which are polygynous, diurnal and open-habitat dwellers. Sexual selection has underpinned many of these changes, which are not necessarily advantageous for individual survival. Domestication has affected certain characteristics, more in terms of their quantitative rather than qualitative expression. However, restrictions imposed by domestication can also affect behaviors such as isolation and post-natal bonding while artificial selection can, by focusing on certain traits, cause unforeseen effects in genetically linked traits, which, when sex-specific or sex-linked, can be reflected in SD. On a global scale, environmental changes can have important phylogenetic implications for species which rely upon environmental cues for activities as migration, hibernation and breeding, especially when SD occurs in response to such cues. Understanding the evolutionary rationale behind the development of SDs, as well as the dynamics which occur at the interface between natural and artificial selection, allows positive insights into areas as diverse as wildlife preservation and livestock management. For both, greatest "success" should be achieved when artificial selection occurs in harmony with natural selection within a supportive environment. Thus the aim of this review is to discuss current knowledge relating to the evolution, benefits and costs of mammalian sexual dimorphisms and, where possible, draw conclusions that might be beneficial for the husbandry and propagation of mammals today.     

Correlated evolution in parental care in females but not males in response to selection on paternity assurance behaviour

According to classical parental care theory males are expected to provide less parental care when offspring in a brood are less likely to be their own, but empirical evidence in support of this relationship is equivocal. Recent work predicts that social interactions between the sexes can modify co‐evolution between traits involved in mating and parental care as a result of costs associated with these social interactions (i.e. sexual conflict). In burying beetles (Nicrophorus vespilloides), we use artificial selection on a paternity assurance trait, and crosses within and between selection lines, to show that selection acting on females, not males, can drive the co‐evolution of paternity assurance traits and parental care. Males do not care more in response to selection on mating rate. Instead, patterns of parental care change as an indirect response to costs of mating for females.