PATERNAL CARE: DIRECT AND INDIRECT GENETIC EFFECTS OF FATHERS ON OFFSPRING PERFORMANCE

Knowledge of how genetic effects arising from parental care influence the evolution of offspring traits comes almost exclusively from studies of maternal care. However, males provide care in some taxa, and often this care differs from females in quality or quantity. If variation in paternal care is genetically based then, like maternal care and maternal effects, paternal effects may have important consequences for the evolution of offspring traits via indirect genetic effects (IGEs). IGEs and direct–indirect genetic covariances associated with parental care can contribute substantially to total heritability and influence predictions about how traits respond to selection. It is unknown, however, if the magnitude and sign of parental effects arising from fathers are the same as those arising from mothers. We used a reciprocal cross‐fostering experiment to quantify environmental and genetic effects of paternal care on offspring performance in the burying beetle, Nicrophorus vespilloides. We found that IGEs were substantial and direct–indirect genetic covariances were negative. Combined, these patterns led to low total heritabilities for offspring performance traits. Thus, under paternal care, offspring performance traits are unlikely to evolve in response to selection, and variation in these traits will be maintained in the population despite potentially strong selection on these traits. These patterns are similar to those generated by maternal care, indicating that the genetic effects of care on offspring performance are independent of the caregiver's sex.     

Phenotypic and genetic integration of personality and growth under competition in the sheepshead swordtail,Xiphophorus birchmanni

Competition for resources including food, physical space, and potential mates is a fundamental ecological process shaping variation in individual phenotype and fitness. The evolution of competitive ability, in particular social dominance, depends on genetic (co)variation among traits causal (e.g., behavior) or consequent (e.g., growth) to competitive outcomes. If dominance is heritable, it will generate both direct and indirect genetic effects (IGE) on resource‐dependent traits. The latter are expected to impose evolutionary constraint because winners necessarily gain resources at the expense of losers. We varied competition in a population of sheepshead swordtails, Xiphophorus birchmanni, to investigate effects on behavior, size, growth, and survival. We then applied quantitative genetic analyses to determine (i) whether competition leads to phenotypic and/or genetic integration of behavior with life history and (ii) the potential for IGE to constrain life history evolution. Size, growth, and survival were reduced at high competition. Male dominance was repeatable and dominant individuals show higher growth and survival. Additive genetic contributions to phenotypic covariance were significant, with the G matrix largely recapitulating phenotypic relationships. Social dominance has a low but significant heritability and is strongly genetically correlated with size and growth. Assuming causal dependence of growth on dominance, hidden IGE will therefore reduce evolutionary potential.     

Indirect genetic effects from ecological interactions in Arabidopsis thaliana

Indirect genetic effects arise when genes expressed in one individual affect the expression of traits in other individuals. The importance of indirect genetic effects has been recognized for a diversity of evolutionary processes including kin selection, sexual selection, community structure and multilevel selection, but data regarding their genetic architecture and prevalence throughout the genome remain scarce, especially for interactions between unrelated individuals. Using a set of 411 Bay-0 x Shahdara Arabidopsis recombinant inbred lines grown with Landsberg neighbours, we examined quantitative trait loci (QTL) having direct and indirect effects on size, developmental, and fitness related traits. Using an interval mapping approach, we identified 15 QTL with direct effects and found that 13 of these QTL had significant indirect effects on trait expression in neighbouring plants. These results suggest widespread pleiotropy, as nearly all direct effect QTL have associated pleiotropic indirect effects. Paradoxically, most indirect effects were of the same sign as direct effects, creating a pattern of nearly universal positive pleiotropy that makes most covariances between direct and indirect effects positive. These results are consistent with a complex genetic basis for intraspecific interactions, but suggest that interactions between neighbouring plants are largely positive, rather than negative as would be expected for competition. In addition to their evolutionary and ecological importance, these pleiotropic relationships between DGE and IGE loci have implications for quantitative genetic studies of natural populations as well as experimental design considerations. Additionally, studies that ignore IGEs may over- or underestimate quantitative genetic parameters, as well as the effect of and variance contributed by QTL.     

Indirect Genetic Effects for Survival in Domestic Chickens (Gallus gallus) Are Magnified in Crossbred Genotypes and Show a Parent-of-Origin Effect

Through social interactions, individuals can affect one another’s phenotype. The heritable effect of an individual on the phenotype of a conspecific is known as an indirect genetic effect (IGE). Although IGEs can have a substantial impact on heritable variation and response to selection, little is known about the genetic architecture of traits affected by IGEs. We studied IGEs for survival in domestic chickens (Gallus gallus), using data on two purebred lines and their reciprocal cross. Birds were kept in groups of four. Feather pecking and cannibalism caused mortality, as beaks were kept intact. Survival time was shorter in crossbreds than in purebreds, indicating outbreeding depression and the presence of nonadditive genetic effects. IGEs contributed the majority of heritable variation in crossbreds (87 and 72%) and around half of heritable variation in purebreds (65 and 44%). There was no evidence of dominance variance, neither direct nor indirect. Absence of dominance variance in combination with considerable outbreeding depression suggests that survival is affected by many loci. Direct–indirect genetic correlations were moderately to highly negative in crossbreds (−0.37 ± 0.17 and −0.83 ± 0.10), but low and not significantly different from zero in purebreds (0.20 ± 0.21 and −0.28 ± 0.18). Consequently, unlike purebreds, crossbreds would fail to respond positively to mass selection. The direct genetic correlation between both crosses was high (0.95 ± 0.23), whereas the indirect genetic correlation was moderate (0.41 ± 0.26). Thus, for IGEs, it mattered which parental line provided the sire and which provided the dam. This indirect parent-of-origin effect appeared to be paternally transmitted and is probably Z chromosome linked.     

Maternal effects and the potential for evolution in a natural population of animals

Maternal effects are widespread and can have dramatic influences on evolutionary dynamics, but their genetic basis has been measured rarely in natural populations. We used cross-fostering techniques and a long-term study of a natural population of red squirrels, Tamiasciurus hudsonicus, to estimate both direct (heritability) and indirect (maternal) influences on the potential for evolution. Juvenile growth in both body mass and size had significant amounts of genetic variation (mass h(2) = 0.10; size h(2) = 0.33), but experienced large, heritable maternal effects. Growth in body mass also had a large positive covariance between direct and maternal genetic effects. The consideration of these indirect genetic effects revealed a greater than three-fold increase in the potential for evolution of growth in body mass (h(2)t = 0.36) relative to that predicted by heritability alone. Simple heritabilities, therefore, may severely underestimate or overestimate the potential for evolution in natural populations of animals.     

Social effects of territorial neighbours on the timing of spring breeding in North American red squirrels

Organisms can affect one another's phenotypes when they socially interact. Indirect genetic effects occur when an individual's phenotype is affected by genes expressed in another individual. These heritable effects can enhance or reduce adaptive potential, thereby accelerating or reversing evolutionary change. Quantifying these social effects is therefore crucial for our understanding of evolution, yet estimates of indirect genetic effects in wild animals are limited to dyadic interactions. We estimated indirect phenotypic and genetic effects, and their covariance with direct effects, for the date of spring breeding in North American red squirrels (Tamiasciurus hudsonicus) living in an array of territories of varying spatial proximity. Additionally, we estimated indirect effects and the strength of selection at low and high population densities. Social effects of neighbours on the date of spring breeding were different from zero at high population densities but not at low population densities. Indirect phenotypic effects accounted for a larger amount of variation in the date of breeding than differences attributable to the among‐individual variance, suggesting social interactions are important for determining breeding dates. The genetic component to these indirect effects was however not statistically significant. We therefore showcase a powerful and flexible method that will allow researchers working in organisms with a range of social systems to estimate indirect phenotypic and genetic effects, and demonstrate the degree to which social interactions can influence phenotypes, even in a solitary species.     

EVOLUTION OF FLORAL TRAITS IN A HERMAPHRODITIC PLANT: FIELD MEASUREMENTS OF HERITABILITIES AND GENETIC CORRELATIONS

Genetic variances, heritabilities, and genetic correlations of floral traits were measured in the monocarpic perennial Ipomopsis aggregata (Polemoniaceae). A paternal half-sib design was employed to generate seeds in each of four years, and seeds were planted back in the field near the parental site. The progeny were followed for up to eight years to estimate quantitative genetic parameters subject to natural levels of environmental variation over the entire life cycle. Narrow-sense heritabilities of 0.2–0.8 were detected for the morphometric traits of corolla length, corolla width, stigma position, and anther position. The proportion of time spent by the protandrous flowers in the pistillate phase (“proportion pistillate”) also exhibited detectable heritability of near 0.3. In contrast, heritability estimates for nectar reward traits were low and not significantly different from zero, due to high environmental variance between and within flowering years. The estimates of genetic parameters were combined with phenotypic selection gradients to predict evolutionary responses to selection mediated by the hummingbird pollinators. One trait, corolla width, showed the potential for a rapid response to ongoing selection through male function, as it experienced both direct selection, by influencing pollen export, and relatively high heritability. Predicted responses were lower for proportion pistillate and corolla length, even though these traits also experienced direct selection. Stigma position was expected to respond positively to indirect selection of proportion pistillate but negatively to selection of corolla length, with the net effect sensitive to variation in the selection estimates. Anther position also was not directly selected but could respond to indirect selection of genetically correlated traits.     

No evidence for an indirect benefit from female mate preference in Arctic charr Salvelinus alpinus,but female ornamentation decreases offspring viability

Female mate choice is considered an important evolutionary agent, but there has been an ongoing debate over the fitness consequences it produces, especially in species that have a resource‐free mating system. We examined a potential fitness benefit resulting from the pre‐spawning mate preference in Arctic charr Salvelinus alpinus, a salmonid fish with no parental care. The females were first allowed to discriminate behaviourally between two males presented to them in a free choice test. We then tested with controlled fertilizations whether the females would accrue indirect genetic benefits for their offspring, as measured by embryonic viability, if they had mated with the male they preferred. Both parental identities influenced offspring survivorship, but the females did not consistently prefer the male which gave her the higher reproductive success. Neither was the degree of male red breeding coloration associated with female preference or the observable genetic quality. In contrast, there was a negative relationship between female coloration and her offspring survivorship, suggesting a significant trade‐off in resource investment between sexual ornamentation and reproduction. To conclude, the potential indirect fitness consequences arising from females' pre‐spawning mate preference seem to be negligible in early stages of development of Arctic charr. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 602–611.     

Inheritance of body size in the Barnacle Goose under different environmental conditions

Heritabilities, genetic variances and covariances for body size traits, i.e. tarsus length, head length and body mass, were estimated under different environmental conditions in a Barnacle Goose (Branta leucopsis) population. Under poor growth conditions, that is, when average body size of fully grown offspring in a given cohort was small, the offspring-parent regressions and full-sib analyses yielded heritability estimates not significantly different from zero. By contrast, when growth conditions were normal or good the heritability estimates were generally significantly positive. Comparisons of genetic covariance estimates indicated that they also differed across the analysed environmental conditions. This result, together with similar results obtained in studies of passerine birds, suggests that genotype-environment interactions might be frequent within the range of environments normally encountered by birds in natural populations. If general, such results might question the validity of assuming approximate constancy of additive genetic variances and covariances over time and environments in evolutionary models.     

EFFECTS OF MATERNAL AND PATERNAL ENVIRONMENT AND GENOTYPE ON OFFSPRING PHENOTYPE IN SOLIDAGO ALTISSIMA L.

To predict the possible evolutionary response of a plant species to a new environment, it is necessary to separate genetic from environmental sources of phenotypic variation. In a case study of the invader Solidago altissima, the influences of several kinds of parental effects and of direct inheritance and environment on offspring phenotype were separated. Fifteen genotypes were crossed in three 5 × 5 diallels excluding selfs. Clonal replicates of the parental genotypes were grown in two environments such that each diallel could be made with maternal/paternal plants from sand/sand, sand/soil, soil/sand, and soil/soil. In a first experiment (1989) offspring were raised in the experimental garden and in a second experiment (1990) in the glasshouse. Parent plants growing in sand invested less biomass in inflorescences but produced larger seeds than parent plants growing in soil. In the garden experiment, phenotypic variation among offspring was greatly influenced by environmental heterogeneity. Direct genetic variation (within diallels) was found only for leaf characters and total leaf mass. Germination probability and early seedling mass were significantly affected by phenotypic differences among maternal plants because of genotype ( genetic maternal effects ) and soil environment ( general environmental maternal effects ). Seeds from maternal plants in sand germinated better and produced bigger seedlings than seeds from maternal plants in soil. They also grew taller with time, probably because competition accentuated the initial differences. Height growth and stem mass at harvest (an integrated account of individual growth history) of offspring varied significantly among crosses within parental combinations ( specific environmental maternal effects ). In the glasshouse experiment, the influence of environmental heterogeneity and competition could be kept low. Except for early characters, the influence of direct genetic variation was large but again leaf characters (= basic module morphology) seemed to be under stricter genetic control than did size characters. Genetic maternal effects, general environmental maternal effects, and specific environmental maternal effects dominated in early characters. The maternal effects were exerted both via seed mass and directly on characters of young offspring. Persistent effects of the general paternal environment ( general environmental paternal effects ) were found for leaf length and stem and leaf mass at harvest. They were opposite in direction to the general environmental maternal effects, that is the same genotypes produced “better mothers” in sand but “better fathers” in soil. The general environmental paternal effects must have been due to differences in pollen quality, resulting from pollen selection within the male parent or leading to pre- or postzygotic selection within the female parent. The ranking of crosses according to mean offspring phenotypes was different in the two experiments, suggesting strong interaction of the observed effects with the environment. The correlation structure among characters changed less between experiments than did the pattern of variation of single characters, but under the competitive conditions in the garden plant height seemed to be more directly related to fitness than in the glasshouse. Reduced competition could also explain why maternal effects were less persistent in the glasshouse than in the garden experiment. Evolution via selection of maternal effects would be possible in the study population because these effects are in part due to genetic differences among parents.     

Direct and indirect phenotypic effects on sociability indicate potential to evolve

The decision to leave or join a group is important as group size influences many aspects of organisms' lives and their fitness. This tendency to socialise with others, sociability, should be influenced by genes carried by focal individuals (direct genetic effects) and by genes in partner individuals (indirect genetic effects), indicating the trait's evolution could be slower or faster than expected. However, estimating these genetic parameters is difficult. Here, in a laboratory population of the cockroach Blaptica dubia, I estimate phenotypic parameters for sociability: repeatability (R) and repeatable influence (RI), that indicate whether direct and indirect genetic effects respectively are likely. I also estimate the interaction coefficient (Ψ), which quantifies how strongly a partner's trait influences the phenotype of the focal individual and is key in models for the evolution of interacting phenotypes. Focal individuals were somewhat repeatable for sociability across a 3-week period (R = 0.080), and partners also had marginally consistent effects on focal sociability (RI = 0.053). The interaction coefficient was non-zero, although in opposite sign for the sexes; males preferred to associate with larger individuals (Ψ_male = −0.129), while females preferred to associate with smaller individuals (Ψ_female = 0.071). Individual sociability was consistent between dyadic trials and in social networks of groups. These results provide phenotypic evidence that direct and indirect genetic effects have limited influence on sociability, with perhaps most evolutionary potential stemming from heritable effects of the body mass of partners. Sex-specific interaction coefficients may produce sexual conflict and the evolution of sexual dimorphism in social behaviour.     

The quantitative genetics of indirect genetic effects: a selective review of modelling issues

Indirect genetic effects (IGE) occur when the genotype of an individual affects the phenotypic trait value of another conspecific individual. IGEs can have profound effects on both the magnitude and the direction of response to selection. Models of inheritance and response to selection in traits subject to IGEs have been developed within two frameworks; a trait-based framework in which IGEs are specified as a direct consequence of individual trait values, and a variance-component framework in which phenotypic variance is decomposed into a direct and an indirect additive genetic component. This work is a selective review of the quantitative genetics of traits affected by IGEs, with a focus on modelling, estimation and interpretation issues. It includes a discussion on variance-component vs trait-based models of IGEs, a review of issues related to the estimation of IGEs from field data, including the estimation of the interaction coefficient Ψ (psi), and a discussion on the relevance of IGEs for response to selection in cases where the strength of interaction varies among pairs of individuals. An investigation of the trait-based model shows that the interaction coefficient Ψ may deviate considerably from the corresponding regression coefficient when feedback occurs. The increasing research effort devoted to IGEs suggests that they are a widespread phenomenon, probably particularly in natural populations and plants. Further work in this field should considerably broaden our understanding of the quantitative genetics of inheritance and response to selection in relation to the social organisation of populations.     

Direct, maternal, and sibsocial genetic effects on individual and colony traits in an ant

When social interactions occur, the phenotype of an individual is influenced directly by its own genes (direct genetic effects) but also indirectly by genes expressed in social partners (indirect genetic effects). Social insect colonies are characterized by extensive behavioral interactions among workers, brood, and queens so that indirect genetic effects are particularly relevant. I used a series of experimental manipulations to disentangle the contribution of direct effects, maternal (queen) effects, and sibsocial (worker) effects to variation for worker, gyne, and male mass; caste ratio; and sex ratio in the ant Temnothorax curvispinosus. The results indicate genetic variance for direct, maternal, and sibsocial effects for all traits, except for male mass there was no significant maternal variance, and for sex ratio the variance for direct effects was not separable from maternal variance for the primary sex ratio. Estimates of genetic correlations between direct, maternal, and sibsocial effects were generally negative, indicating that these effects may not evolve independently. These results have broad implications for social insect evolution. For example, the genetic architecture underlying social insect traits may constrain the realization of evolutionary conflicts between social partners.     

THE QUANTITATIVE GENETICS AND COEVOLUTION OF MALE AND FEMALE REPRODUCTIVE TRAITS

Studies of experimental sexual selection have tested the effect of variation in the intensity of sexual selection on male investment in reproduction, particularly sperm. However, in several species, including Drosophila pseudoobscura, no sperm response to experimental evolution has occurred. Here, we take a quantitative genetics approach to examine whether genetic constraints explain the limited evolutionary response. We quantified direct and indirect genetic variation, and genetic correlations within and between the sexes, in experimental populations of D. pseudoobscura. We found that sperm number may be limited by low heritability and evolvability whereas sperm quality (length) has moderate V_A and CV_A but does not evolve. Likewise, the female reproductive tract, suggested to drive the evolution of sperm, did not respond to experimental sexual selection even though there was sufficient genetic variation. The lack of genetic correlations between the sexes supports the opportunity for sexual conflict over investment in sperm by males and their storage by females. Our results suggest no absolute constraint arising from a lack of direct or indirect genetic variation or patterns of genetic covariation. These patterns show why responses to experimental evolution are hard to predict, and why research on genetic variation underlying interacting reproductive traits is needed.     

Quantitative genetics of growth and development time in the burying beetle Nicrophorus pustulatus in the presence and absence of post-hatching parental care

Despite a growing interest in the evolutionary aspects of maternal effects, few studies have examined the genetic consequences of maternal effects associated with parental care. To begin to provide data on nonlaboratory or nondomestic animals, we compared the effect of presence and absence of parental care on phenotype expression of larval mass and development time at different life-history stages in the burying beetle Nicrophorus pustulatus. This beetle has facultative care; parents can feed their larvae through regurgitation of digested carrion or offspring can feed by themselves from previously prepared carrion. To investigate larval responses to these two levels of care, including estimates of additive genetic effects, maternal effects, and genotype-by-environment interactions, we used a half-sibling split-family breeding experiment-raising half of the offspring of a family in the presence of their mother and the other half without their mother present. Larvae reared with their mother present were on average heavier and developed faster, although some of the differences in development decreased or were eliminated by the adult stage. These results suggest that presence or absence of post-hatching maternal care plays an important role in phenotype expression early in life, whereas later the phenotype of the offspring is determined mainly by the genotype and/or unshared environmental effects. Our study also permitted us to examine the differences in genetic effects between the two care environments. Heritabilities, maternal/common environment effect, and most genetic correlations did not differ between the care treatments. Genetic analyses revealed substantial additive genetic effects for development time but small effects for measures of body mass. Maternal plus common environment effects were high for measures of mass but low for development time, suggesting that indirect genetic effects of maternal and/or common environment are less important for the evolution of development time than for mass. Estimates of genetic correlations revealed a trade-off between the duration of the two development stages after the offspring left the carrion. There was also a negative genetic correlation between the time spent on carrion and the mass at 72 h, when mothers usually stop feeding. The analysis of genotype-by-environment interactions indicates substantial variation among maternal families in response to care. Presence or absence of parental care may therefore contribute to the additive genetic variance through its interaction with the maternal component of the additive genetic variance. The presence of this interaction further suggests that parents may vary in care strategies, with some parents dispersing after preparation of the carrion and some parents staying with the larvae. This interaction may help maintain genetic variation in growth, development time, and parental care behavior. Additional work is needed, however, to quantify indirect genetic effects and genetic variation in parental care behavior itself.     

Complex genotype interactions influence social fitness during the developmental phase of the social amoeba Dictyostelium discoideum

When individuals interact, phenotypic variation can be partitioned into direct genetic effects (DGEs) of the individuals’ own genotypes, indirect genetic effects (IGEs) of their social partners’ genotypes and epistatic interactions between the genotypes of interacting individuals (‘genotype‐by‐genotype (G×G) epistasis’). These components can all play important roles in evolutionary processes, but few empirical studies have examined their importance. The social amoeba Dictyostelium discoideum provides an ideal system to measure these effects during social interactions and development. When starved, free‐living amoebae aggregate and differentiate into a multicellular fruiting body with a dead stalk that holds aloft viable spores. By measuring interactions among a set of natural strains, we quantify DGEs, IGEs and G×G epistasis affecting spore formation. We find that DGEs explain most of the phenotypic variance (57.6%) whereas IGEs explain a smaller (13.3%) but highly significant component. Interestingly, G×G epistasis explains nearly a quarter of the variance (23.0%), highlighting the complex nature of genotype interactions. These results demonstrate the large impact that social interactions can have on development and suggest that social effects should play an important role in developmental evolution in this system.     

Genetic architecture of survival and fitness-related traits in two populations of Atlantic salmon

The additive genetic effects of traits can be used to predict evolutionary trajectories, such as responses to selection. Non-additive genetic and maternal environmental effects can also change evolutionary trajectories and influence phenotypes, but these effects have received less attention by researchers. We partitioned the phenotypic variance of survival and fitness-related traits into additive genetic, non-additive genetic and maternal environmental effects using a full-factorial breeding design within two allopatric populations of Atlantic salmon (Salmo salar). Maternal environmental effects were large at early life stages, but decreased during development, with non-additive genetic effects being most significant at later juvenile stages (alevin and fry). Non-additive genetic effects were also, on average, larger than additive genetic effects. The populations, generally, did not differ in the trait values or inferred genetic architecture of the traits. Any differences between the populations for trait values could be explained by maternal environmental effects. We discuss whether the similarities in architectures of these populations is the result of natural selection across a common juvenile environment.     

Evolutionary quantitative genetics of nonlinear developmental systems

In quantitative genetics, the effects of developmental relationships among traits on microevolution are generally represented by the contribution of pleiotropy to additive genetic covariances. Pleiotropic additive genetic covariances arise only from the average effects of alleles on multiple traits, and therefore the evolutionary importance of nonlinearities in development is generally neglected in quantitative genetic views on evolution. However, nonlinearities in relationships among traits at the level of whole organisms are undeniably important to biology in general, and therefore critical to understanding evolution. I outline a system for characterizing key quantitative parameters in nonlinear developmental systems, which yields expressions for quantities such as trait means and phenotypic and genetic covariance matrices. I then develop a system for quantitative prediction of evolution in nonlinear developmental systems. I apply the system to generating a new hypothesis for why direct stabilizing selection is rarely observed. Other uses will include separation of purely correlative from direct and indirect causal effects in studying mechanisms of selection, generation of predictions of medium‐term evolutionary trajectories rather than immediate predictions of evolutionary change over single generation time‐steps, and the development of efficient and biologically motivated models for separating additive from epistatic genetic variances and covariances.     

Effects of parental care on the accumulation and release of cryptic genetic variation: <Emphasis Type="Italic">review of mechanisms and a case study of dung beetles</Emphasis>

Cryptic genetic variation plays an important role in the emergence of disease and evolutionary responses to environmental change. Focusing on parental care behavior, we discuss three mechanisms by which behavior can affect the accumulation and release of cryptic genetic variation. We illustrate how these hypotheses might be tested with preliminary data from Onthophagus dung beetles, which provide indirect parental care by provisioning their offspring with dung and sheltering them underground. The environmental stress hypothesis states that parental care reduces selection intensity on novel mutations when increased parental care results in a less stressful offspring environment. A review of recent literature, coupled with an irradiation experiment in beetles, suggests this mechanism may operate in some situations, but depends on the types of mutations under consideration. The relaxed selection hypothesis states that genes expressed in low care environments should be under weakened selection because their phenotypic manifestations are exposed to selection less frequently, and thus are prone to mutation accumulation. If parental care is reduced, for instance due to population-wide environmental changes, such cryptic variation may exert phenotypic effects, becoming exposed to selection. There is substantial theory in support of this hypothesis, and comparisons between beetle populations that differ in parental care behavior further support this idea. Finally, the compensation hypothesis states that organisms with direct parental care may be able to respond to cues or signals from offspring and compensate for genetic variants. We highlight the extensive discussion of this hypothesis with respect to medical care and genetic load in humans and explore invertebrate systems that may constitute powerful models for further inquiry. In summary, several mechanisms exist by which care behavior may shape the accumulation and release of cryptic genetic variation, thereby affecting the potential emergence of diseases and the rate and direction of evolutionary responses to novel environments.     

When mother knows best: A population genetic model of transgenerational versus intragenerational plasticity

Many organisms exhibit phenotypic plasticity; producing alternate phenotypes depending on the environment. Individuals can be plastic (intragenerational or direct plasticity), wherein individuals of the same genotype produce different phenotypes in response to the environments they experience. Alternatively, an individual's phenotype may be under the control of its parents, usually the mother (transgenerational or indirect plasticity), so that mother's genotype determines the phenotype produced by a given genotype of her offspring. Under what conditions does plasticity evolve to have intragenerational as opposed to transgenerational genetic control? To explore this question, we present a population genetic model for the evolution of transgenerational and intragenerational plasticity. We hypothesize that the capacity for plasticity incurs a fitness cost, which is borne either by the individual developing the plastic phenotype or by its mother. We also hypothesize that individuals are imperfect predictors of future environments and their capacity for plasticity can lead them occasionally to make a low‐fitness phenotype for a particular environment. When the cost, benefit and error parameters are equal, we show that there is no evolutionary advantage to intragenerational over transgenerational plasticity, although the rate of evolution of transgenerational plasticity is half the rate for intragenerational plasticity, as predicted by theory on indirect genetic effects. We find that transgenerational plasticity evolves when mothers are better predictors of future environments than offspring or when the fitness cost of the capacity for plasticity is more readily borne by a mother than by her developing offspring. We discuss different natural systems with either direct intragenerational plasticity or indirect transgenerational plasticity and find a pattern qualitatively in accord with the predictions of our model.