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.     

Who listens to mother? A whole-family perspective on the evolution of maternal hormone allocation

Maternal effects, or the influence of maternal environment and phenotype on offspring phenotype, may allow mothers to fine-tune their offspring's developmental trajectory and resulting phenotype sometimes long after the offspring has reached independence. However, maternal effects on offspring phenotype do not evolve in isolation, but rather within the context of a family unit, where the separate and often conflicting evolutionary interests of mothers, fathers and offspring are all at play. While intrafamilial conflicts are routinely invoked to explain other components of reproductive strategy, remarkably little is known about how intrafamilial conflicts influence maternal effects. We argue that much of the considerable variation in the relationship between maternally derived hormones, nutrients and other compounds and the resulting offspring phenotype might be explained by the presence of conflicting selection pressures on different family members. In this review, we examine the existing literature on maternal hormone allocation as a case study for maternal effects more broadly, and explore new hypotheses that arise when we consider current findings within a framework that explicitly incorporates the different evolutionary interests of the mother, her offspring and other family members. Specifically, we hypothesise that the relationship between maternal hormone allocation and offspring phenotype depends on a mother's ability to manipulate the signals she sends to offspring, the ability of family members to be plastic in their response to those signals and the capacity for the phenotypes and strategies of various family members to interact and influence one another on both behavioural and evolutionary timescales. We also provide suggestions for experimental, comparative and theoretical work that may be instrumental in testing these hypotheses. In particular, we highlight that manipulating the level of information available to different family members may reveal important insights into when and to what extent maternal hormones influence offspring development. We conclude that the evolution of maternal hormone allocation is likely to be shaped by the conflicting fitness optima of mothers, fathers and offspring, and that the outcome of this conflict depends on the relative balance of power between family members. Extending our hypotheses to incorporate interactions between family members, as well as more complex social groups and a wider range of taxa, may provide exciting new developments in the fields of endocrinology and maternal effects.     

Mother’s curse and indirect genetic effects: Do males matter to mitochondrial genome evolution?

Maternal inheritance of mitochondrial DNA (mtDNA) was originally thought to prevent any response to selection on male phenotypic variation attributable to mtDNA, resulting in a male‐biased mtDNA mutation load (“mother's curse”). However, the theory underpinning this claim implicitly assumes that a male's mtDNA has no effect on the fitness of females he comes into contact with. If such “mitochondrially encoded indirect genetics effects” (mtIGEs) do in fact exist, and there is relatedness between the mitochondrial genomes of interacting males and females, male mtDNA‐encoded traits can undergo adaptation after all. We tested this possibility using strains of Drosophila melanogaster that differ in their mtDNA. Our experiments indicate that female fitness is influenced by the mtDNA carried by males that the females encounter, which could plausibly allow the mitochondrial genome to evolve via kin selection. We argue that mtIGEs are probably common, and that this might ameliorate or exacerbate mother's curse.     

Idiosyncratic evolution of maternal effects in response to juvenile malnutrition in Drosophila

Maternal effects often affect fitness traits, but there is little experimental evidence pertaining to their contribution to response to selection imposed by novel environments. We studied the evolution of maternal effects in Drosophila populations selected for tolerance to chronic larval malnutrition. To this end, we performed pairwise reciprocal F₁ crosses between six selected (malnutrition tolerant) populations and six unselected control populations and assessed the effect of cross direction on larval growth and developmental rate, adult weight and egg‐to‐adult viability expressed under the malnutrition regime. Each pair of reciprocal crosses revealed large maternal effects (possibly including cytoplasmic genetic effects) on at least one trait, but the magnitude, sign and which traits were affected varied among populations. Thus, maternal effects contributed significantly to the response to selection imposed by the malnutrition regime, but these changes were idiosyncratic, suggesting a rugged adaptive landscape. Furthermore, although the selected populations evolved both faster growth and higher viability, the maternal effects on growth rate and viability were negatively correlated across populations. Thus, genes mediating maternal effects can evolve to partially counteract the response to selection mediated by the effects of alleles on their own carriers’ phenotype, and maternal effects may contribute to evolutionary trade‐offs between components of offspring fitness.     

SELECTION ON MOTHERS AND OFFSPRING: WHOSE PHENOTYPE IS IT AND DOES IT MATTER?

Reproductive and early life-history traits can be considered aspects of either offspring or maternal phenotype, and their evolution will therefore depend on selection operating through offspring and maternal components of fitness. Furthermore, selection at these levels may be antagonistic, with optimal offspring and maternal fitness occurring at different phenotypic values. We examined selection regimes on the correlated traits of birth weight, birth date, and litter size in Soay sheep (Ovis aries) using data from a long-term study of a free-living population on the archipelago of St. Kilda, Scotland. We tested the hypothesis that selective constraints on the evolution of the multivariate phenotype arise through antagonistic selection, either acting at offspring and maternal levels, or on correlated aspects of phenotype. All three traits were found to be under selection through variance in short-term and lifetime measures of fitness. Analysis of lifetime fitness revealed strong positive directional selection on birth weight and weaker selection for increased birth date at both levels. However, there was also evidence for stabilizing selection on these traits at the maternal level, with reduced fitness at high phenotypic values indicating lower phenotypic optima for mothers than for offspring. Additionally, antagonistic selection was found on litter size. From the offspring's point of view it is better to be born a singleton, whereas maternal fitness increases with average litter size. The decreased fitness of twins is caused by their reduced birth weight; therefore, this antagonistic selection likely results from trade-offs between litter size and birth weight that have different optimal resolutions with respect to offspring and maternal fitness. Our results highlight how selection regimes may vary depending on the assignment of reproductive and early life-history traits to either offspring or maternal phenotype.     

THE COADAPTATION OF PARENTAL AND OFFSPRING CHARACTERS

Parents often have important influences on their offspring's traits and/or fitness (i.e., maternal or paternal effects). When offspring fitness is determined by the joint influences of offspring and parental traits, selection may favor particular combinations that generate high offspring fitness. We show that this epistasis for fitness between the parental and offspring genotypes can result in the evolution of their joint distribution, generating genetic correlations between the parental and offspring characters. This phenomenon can be viewed as a coadaptive process in which offspring genotypes evolve to function with the parentally provided environment and, in turn, the genes for this environment become associated with specific offspring genes adapted to it. To illustrate this point, we present two scenarios in which selection on offspring alone alters the correlation between a maternal and an offspring character. We use a quantitative genetic maternal effect model combined with a simple quadratic model of fitness to examine changes in the linkage disequilibrium between the maternal and offspring genotypes. In the first scenario, stabilizing selection on a maternally affected offspring character results in a genetic correlation that is opposite in sign to the maternal effect. In the second scenario, directional selection on an offspring trait that shows a nonadditive maternal effect can result in selection for positive covariances between the traits. This form of selection also results in increased genetic variation in maternal and offspring characters, and may, in the extreme case, promote host-race formation or speciation. This model provides a possible evolutionary explanation for the ubiquity of large genetic correlations between maternal and offspring traits, and suggests that this pattern of coinheritance may reflect functional relationships between these characters (i.e., functional integration).     

Maternal environmental effects of competition influence evolutionary potential in rapeseed (<Emphasis Type="Italic">Brassica</Emphasis><Emphasis Type="Italic">rapa</Emphasis>)

Maternal environmental effects reflect the contribution of the maternal environment to the offspring phenotype. Maternal effects are prevalent in plants and animals and may undergo adaptive evolution and affect patterns of natural selection within and across generations. Here, we raise two generations of a rapeseed (Brassica rapa) population derived from a cross between a rapid-cycling and an oilseed genotype in competitive and noncompetitive settings. Maternal environment had little effect on average offspring phenotypes. Maternal genotypes, however, differed in the sensitivity of almost all offspring phenotypes to the maternal environment, demonstrating genetic variation in maternal effects for traits expressed throughout ontogeny. Maternal environment did not significantly affect progeny seed production, and maternal genotypes were not variable for this trait, indicating no evidence for direct maternal effects on offspring fitness. Maternal environment influenced natural selection in the progeny generation; disruptive selection acted on seed mass among seeds matured in the noncompetitive maternal environment versus no significant selection on this trait for seeds matured in the competitive maternal environment. Although maternal effects did not directly increase fitness, they did affect evolutionary potential and selection in the progeny generation. These results suggest that diverse phenotypes of both wild and cultivated B. rapa genotypes will depend on the maternal environment in which the seeds are matured.     

The nature of nurture in a wild mammal's fitness

Genetic variation in fitness is required for the adaptive evolution of any trait but natural selection is thought to erode genetic variance in fitness. This paradox has motivated the search for mechanisms that might maintain a population''s adaptive potential. Mothers make many contributions to the attributes of their developing offspring and these maternal effects can influence responses to natural selection if maternal effects are themselves heritable. Maternal genetic effects (MGEs) on fitness might, therefore, represent an underappreciated source of adaptive potential in wild populations. Here we used two decades of data from a pedigreed wild population of North American red squirrels to show that MGEs on offspring fitness increased the population''s evolvability by over two orders of magnitude relative to expectations from direct genetic effects alone. MGEs are predicted to maintain more variation than direct genetic effects in the face of selection, but we also found evidence of maternal effect trade-offs. Mothers that raised high-fitness offspring in one environment raised low-fitness offspring in another environment. Such a fitness trade-off is expected to maintain maternal genetic variation in fitness, which provided additional capacity for adaptive evolution beyond that provided by direct genetic effects on fitness.     

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.     

A theoretical model of the evolution of maternal effects under parent-offspring conflict

The evolution of maternal effects on offspring phenotype should depend on the extent of parent-offspring conflict and costs and constraints associated with maternal and offspring strategies. Here, we develop a model of maternal effects on offspring dispersal phenotype under parent-offspring conflict to evaluate such dependence. In the absence of evolutionary constraints and costs, offspring evolve dispersal rates from different patch types that reflect their own, rather than the maternal, optima. This result also holds true when offspring are unable to assess their own environment because the maternal phenotype provides an additional source of information. Consequently, maternal effects on offspring diapause, dispersal, and other traits that do not necessarily represent costly resource investment are more likely to maximize offspring than maternal fitness. However, when trait expression was costly, the evolutionarily stable dispersal rates tended to deviate from those under both maternal and offspring control. We use our results to (re)interpret some recent work on maternal effects and their adaptive value and provide suggestions for future work.     

A unified approach to the evolutionary consequences of genetic and nongenetic inheritance

Inheritance-the influence of ancestors on the phenotypes of their descendants-translates natural selection into evolutionary change. For the past century, inheritance has been conceptualized almost exclusively as the transmission of DNA sequence variation from parents to offspring in accordance with Mendelian rules, but advances in cell and developmental biology have now revealed a rich array of inheritance mechanisms. This empirical evidence calls for a unified conception of inheritance that combines genetic and nongenetic mechanisms and encompasses the known range of transgenerational effects, including the transmission of genetic and epigenetic variation, the transmission of plastic phenotypes (acquired traits), and the effects of parental environment and genotype on offspring phenotype. We propose a unified theoretical framework based on the Price equation that can be used to model evolution under an expanded inheritance concept that combines the effects of genetic and nongenetic inheritance. To illustrate the utility and generality of this framework, we show how it can be applied to a variety of scenarios, including nontransmissible environmental noise, maternal effects, indirect genetic effects, transgenerational epigenetic inheritance, RNA-mediated inheritance, and cultural inheritance.     

The effect of maternal glucocorticoid levels on juvenile docility in yellow-bellied marmots

Maternal effects can have significant and long-term consequences on offspring behavior and survival, while consistent individual differences (i.e., personality) can have profound impacts on individual fitness. Thus, both can influence population dynamics. However, the underlying mechanisms that determine variation in personality traits are poorly understood. Maternal effects are one potential mechanism that may explain personality variation. We capitalized on a long-term study of yellow-bellied marmots (Marmota flaviventris) to identify maternal effects on juvenile docility. To do so, we partitioned the variance in juvenile docility using a quantitative genetic modeling approach to isolate potential maternal effects. We also directly tested whether maternal stress, measured through fecal glucocorticoid metabolite levels during lactation of 82 mothers, was associated with offspring docility. Docility scores were estimated for 645 juveniles trapped between 2002 and 2012. We found an interaction between maternal glucocorticoid levels and dam age on juvenile docility. We also found significant maternal, litter, permanent environment, and year effects. These results suggest that a mother's life history stage interacts with stress to influence offspring personality. This early life influence can have long lasting effects on an individual's docility throughout life.     

Can paternal leakage maintain sexually antagonistic polymorphism in the cytoplasm?

A growing number of studies in multicellular organisms highlight low or moderate frequencies of paternal transmission of cytoplasmic organelles, including both mitochondria and chloroplasts. It is well established that strict maternal inheritance is selectively blind to cytoplasmic elements that are deleterious to males – ’mother's curse’. But it is not known how sensitive this conclusion is to slight levels of paternal cytoplasmic leakage. We assess the scope for polymorphism when individuals bear multiple cytoplasmic alleles in the presence of paternal leakage, bottlenecks and recurrent mutation. When fitness interactions among cytoplasmic elements within an individual are additive, we find that sexually antagonistic polymorphism is restricted to cases of strong selection on males. However, when fitness interactions among cytoplasmic elements are nonlinear, much more extensive polymorphism can be supported in the cytoplasm. In particular, mitochondrial mutants that have strong beneficial fitness effects in males and weak deleterious fitness effects in females when rare (i.e. ’reverse dominance’) are strongly favoured under paternal leakage. We discuss how such epistasis could arise through preferential segregation of mitochondria in sex‐specific somatic tissues. Our analysis shows how paternal leakage can dampen the evolution of deleterious male effects associated with predominant maternal inheritance of cytoplasm, potentially explaining why ’mother's curse’ is less pervasive than predicted by earlier work.     

The Evolution of Multivariate Maternal Effects

There is a growing interest in predicting the social and ecological contexts that favor the evolution of maternal effects. Most predictions focus, however, on maternal effects that affect only a single character, whereas the evolution of maternal effects is poorly understood in the presence of suites of interacting traits. To overcome this, we simulate the evolution of multivariate maternal effects (captured by the matrix M) in a fluctuating environment. We find that the rate of environmental fluctuations has a substantial effect on the properties of M: in slowly changing environments, offspring are selected to have a multivariate phenotype roughly similar to the maternal phenotype, so that M is characterized by positive dominant eigenvalues; by contrast, rapidly changing environments favor Ms with dominant eigenvalues that are negative, as offspring favor a phenotype which substantially differs from the maternal phenotype. Moreover, when fluctuating selection on one maternal character is temporally delayed relative to selection on other traits, we find a striking pattern of cross-trait maternal effects in which maternal characters influence not only the same character in offspring, but also other offspring characters. Additionally, when selection on one character contains more stochastic noise relative to selection on other traits, large cross-trait maternal effects evolve from those maternal traits that experience the smallest amounts of noise. The presence of these cross-trait maternal effects shows that individual maternal effects cannot be studied in isolation, and that their study in a multivariate context may provide important insights about the nature of past selection. Our results call for more studies that measure multivariate maternal effects in wild populations.     

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.     

Polyandry, life-history trade-offs and the evolution of imprinting at Mendelian loci

Genomic imprinting causes parental origin-dependent differential expression of a small number of genes in mammalian and angiosperm plant embryos, resulting in non-Mendelian inheritance of phenotypic traits. The "conflict" theory of the evolution of imprinting proposes that reduced genetic relatedness of paternally, relative to maternally, derived alleles in offspring of polygamous females supports parental sex-specific selection at gene loci that influence maternal investment. While the theory's physiological predictions are well supported by observation, the requirement of polyandry in the evolution of imprinting from an ancestral Mendelian state has not been comprehensively analyzed. Here, we use diallelic models to examine the influence of various degrees of polyandry on the evolution of both Mendelian and imprinted autosomal gene loci that influence trade-offs between maternal fecundity and offspring viability. We show that, given a plausible assumption on the physiological relationship between maternal fecundity and offspring viability, low levels of polyandry are sufficient to reinforce exclusively the fixation of "greedy" paternally imprinted alleles that increase offspring viability at the expense of maternal fecundity and "thrifty" maternally imprinted alleles of opposite effect. We also show that, for all levels of polyandry, Mendelian alleles at genetic loci that influence the trade-off between maternal fecundity and offspring viability reach an evolutionary stable state, whereas pairs of reciprocally imprinted alleles do not.     

Epigenetic effects of infection on the phenotype of host offspring: parasites reaching across host generations

Parasite‐induced changes in host phenotype are now well‐documented from a wide range of taxa. There is a growing body of evidence indicating that parasites can also have trans‐generational consequences, with infection of a host leading to changes in the phenotype of its offspring, though the latter are not parasitised. Several proximate mechanisms have been put forward to explain these ‘maternal’ effects, most involving hormonal or other physiological pathways, ultimately leading to offspring that are pre‐adapted to the parasites they are most likely to encounter based on their mother's experience. Here, we propose that all these trans‐generational effects on offspring phenotype must involve epigenetic phenomena. Epigenetics concerns the appearance and inheritance of seemingly new phenotypic traits without changes in the underlying DNA sequence. Since diet and other environmental factors experienced by a mother can affect gene expression in her offspring by turning genes ‘on’ or ‘off’ (for example, via DNA methylation), why couldn't parasites do it? Although epigenetic effects have not been explicitly invoked to account for trans‐generational impacts of parasites on the phenotype of host offspring, the existing evidence is fully compatible with their involvement. We argue that epigenetic mechanisms must play a central role; we also discuss their evolutionary implications and suggest questions for future investigations in this new and exciting research direction.     

Density-dependent processes influencing the evolutionary dynamics of dispersal: a functional analysis of seed dispersal in Arabidopsis thaliana (Brassicaceae)

We conducted a functional analysis of seed dispersal and its plasticity in response to density in Arabidopsis thaliana by growing morphologically diverse ecotypes under high and low density and measuring seed dispersion patterns under controlled conditions. Maternal plant architectural traits such as height and branching, and fruit traits such as dehiscence and silique length influenced various measures of seed dispersion patterns, including the average dispersal distance, kurtosis of the seed dispersion pattern, and post-dispersal seed density. The density at which plants grew determined which traits influenced dispersal. A change in density would therefore change which maternal characters would be subjected to natural selection through selection on dispersal. Density-mediated maternal effects on dispersal contributed to a negative correlation between parents and offspring for sibling density after dispersal, which could impede the response to selection on post-dispersal sibling density. Plant traits that influenced dispersal also influenced maternal fitness- sometimes opposing selection on dispersal and sometimes augmenting it-and the direction of the relationship sometimes depended on density. These density-dependent relationships between plant traits, dispersal, and maternal fitness can increase or reduce evolutionary constraints on dispersal, depending on the trait and depending on post-dispersal density itself.     

Seed Dispersal as a Maternally Influenced Character: Mechanistic Basis of Maternal Effects and Selection on Maternal Characters in an Annual Plant

Maternal influences on progeny characters affect phenotypic correlations between characters expressed in maternal and progeny generations and consequently influence evolutionary responses to selection. Net selection on maternally influenced characters depends on selection both on the progeny character and on the maternal characters that influence it. I used seed dispersal in Cakile edentula as a system in which to identify the mechanisms of environmentally mediated maternal effects and to determine how selection on maternal characters alters the adaptive value of dispersal. In C. edentula, maternal morphology responds to conspecific density experienced by the mother. Maternal morphology in turn affects offspring (seed) dispersal and density and thereby offspring morphology and fitness. I estimated the magnitude of density-mediated maternal effects on dispersal and identified their mechanism by characterizing the plasticity of maternal morphology to density. I also measured density-dependent selection on maternal characters that influence dispersal. Maternal plasticity to density was caused by both allometric and nonallometric variation in morphology, and this plasticity resulted in a negative correlation between maternal and progeny density. Such negative maternal effects are expected to retard responses to selection. Maternal morphology influenced maternal fitness, in part through the relationship of fitness to maternal plant size and in part through size-independent fitness effects. Maternal phenotypes that promote dispersal, and thereby increase progeny fitness, were associated with decreased maternal fitness. Selection on dispersal at the level of progeny favors increased dispersal; maternal influences on dispersal, however, not only cause a greatly reduced adaptive value of dispersal but lead to the prediction of a slower response to selection.     

Cultural transmission can inhibit the evolution of altruistic helping

The study of culturally inherited traits has led to the suggestion that the evolution of helping behaviors is more likely with cultural transmission than without. Here we evaluate this idea through a comparative analysis of selection on helping under both genetic and cultural inheritance. We develop two simple models for the evolution of helping through cultural group selection: one in which selection on the trait depends solely on Darwinian fitness effects and one in which selection is driven by nonreproductive factors, specifically imitation of strategies achieving higher payoffs. We show that when cultural variants affect Darwinian fitness, the selection pressure on helping can be markedly increased relative to that under genetic transmission. By contrast, when variants are driven by nonreproductive factors, the selection pressure on helping may be reduced relative to that under genetic inheritance. This occurs because, unlike biological offspring, the spread of cultural variants from one group to another through imitation does not reduce the number of these variants in the source group. As a consequence, there is increased within-group competition associated with traits increasing group productivity, which reduces the benefits of helping. In these cases, selection for harming behavior (decreasing the payoff to neighbors) may occur rather than selection for helping.