Antagonistic Parent-Offspring Co-Adaptation

Background

In species across taxa, offspring have means to influence parental investment (PI). PI thus evolves as an interacting phenotype and indirect genetic effects may strongly affect the co-evolutionary dynamics of offspring and parental behaviors. Evolutionary theory focused on explaining how exaggerated offspring solicitation can be understood as resolution of parent-offspring conflict, but the evolutionary origin and diversification of different forms of family interactions remains unclear.

Methodology/Principal Findings

In contrast to previous theory that largely uses a static approach to predict how “offspring individuals” and “parental individuals” should interact given conflict over PI, we present a dynamic theoretical framework of antagonistic selection on the PI individuals obtain/take as offspring and the PI they provide as parents to maximize individual lifetime reproductive success; we analyze a deterministic and a stochastic version of this dynamic framework. We show that a zone for equivalent co-adaptation outcomes exists in which stable levels of PI can evolve and be maintained despite fast strategy transitions and ongoing co-evolutionary dynamics. Under antagonistic co-adaptation, cost-free solicitation can evolve as an adaptation to emerging preferences in parents.

Conclusions/Significance

We show that antagonistic selection across the offspring and parental life-stage of individuals favors co-adapted offspring and parental behavior within a zone of equivalent outcomes. This antagonistic parent-offspring co-adaptation does not require solicitation to be costly, allows for rapid divergence and evolutionary novelty and potentially explains the origin and diversification of the observed provisioning forms in family life.     

Models of parent-offspring conflict. IV. Suppression: Evolutionary retaliation by the parent

We have earlier analysed ESSs for the amount of parental investment (PI) that offspring are expected to solicit from their parents, given that parents acquiesce to offspring demands. The present paper considers evolutionary retaliation by the parent for species where only one parent provides PI. Two genetic loci are envisaged: one (the ‘conflictor’ locus) determines the extent of offspring solicitation; the other (the ‘suppressor’ locus) determines how parents retaliate. Solicitation is assumed to carry a cost which may affect a particular offspring uniquely if time and energy are the major costs, or may affect all offspring in a brood equally if the main cost is predation risk. Two kinds of parental retaliation are possible. Parents may supply PI in proportion to offspring demands, or may ignore solicitation altogether and give a fixed PI. Analytical models of conflict in which the parent supplies PI in proportion to solicitation yield pure ESSs with PI at a compromise level between parent and offspring interests. These are termed ‘pro rata’ ESSs. Where solicitation costs are high, an ‘offspring wins’ ESS (offspring get all they ‘want’) is possible especially for forms of conflict that affect future sibs, and a ‘parent wins’ ESS (parent supplies its optimum) is possible especially for conflict that affects contemporary sibs. When parental retaliation takes the form of ignoring offspring solicitation, this can lead to a ‘parent wins’ ESS if costs of ignoring solicitation are negligible, but where parental insensitivity carries costs, the result is an unresolvable evolutionary chase with cycling frequencies of alleles coding for parent and offspring strategies. ‘Pro rata’ ESSs cannot be invaded by ‘ignore solicitation’ mutants but ‘pro rata’ mutants can often invade at certain stages in ‘ignore solicitation’ limit cycles. We therefore conclude that the probable evolutionary end product for most species will be the ‘pro rata’ ESS in which the parent supplies more PI than would be optimal in the absence of conflict, but less PI than would be an ESS for the offspring in the absence of parental retaliation. Such ESSs will be characterized by solicitation costs; offspring will ‘ask’ for more PI than they get. In nature, under similar conditions, highest conflict will occur when both parents sustain equally the effects of conflict, or when conflict affects contemporary rather than future sibs.     

Parental investment and family dynamics: interactions between theory and empirical tests

The pattern of parental investment (PI) seen in nature is a product of the simultaneous resolution of conflicts of interest between the members of a family. How these conflicts are resolved depends upon the mating system, the genetic mechanism, on whether extra PI affects current or future offspring, and the behavioural mechanisms underlying supply and demand of PI. Until recently very little empirical work has been done to underpin these key determinants of conflict resolution. This review examines recent empirical progress in understanding both (1) how conflict is resolved and (2) its evolutionary consequences. How offspring demand interacts with parental supply of resources determines how conflict is resolved. Two extremes are: passive parental choice of competing offspring, relating to offspring control of resource allocation, and active parental choice relating to parental control. Although most previous empirical work has tended to conclude or assume that parents primarily control resource allocation decisions, recent studies explicitly examining predictions from theoretical analyses have shown that offspring control of resource allocation is more important than previously realised. The amount of PI supplied at resolution depends not on who controls food allocation, however, but on the nature of the supply and demand mechanisms. These have yet to be established experimentally, but a recent regression model illustrates how this could be achieved in the field. Determination of the effect of supply on demand (ESD) and the effect of demand on supply (EDS) mechanisms is critical to parent–offspring conflict theory, which has not been adequately tested empirically. There is an underlying, and until recently untested, assumption of models of intrafamilial conflict that there is genetic variation for both offspring demand and parental supply behaviours, so that the behaviours can coevolve. Recent studies on great tits, burrower bugs and mice all found evidence for genetic variation in supply and demand behaviours, but the predicted negative correlation between genes expressed in mothers and their offspring (i.e. parent–offspring coevolution), was found only for burrower bugs. The lack of a negative relationship for great tits and mice may have been a consequence of antagonistic coevolution between the sexes (sexual conflict). These studies illustrate the importance of the underlying genetics and mating system in determining conflict resolution, and point to the need for new models (especially of interbrood competition) taking differences in the genetics and the co-evolution of the ESD and EDS mechanisms into account. We also discuss the importance of the comparative approach in determining evolutionary consequences of conflicts, and use the recent work on growth costs of begging to illustrate the difficulties of measuring costs of conflict in an evolutionary currency. The recent growth in empirical work on conflicts in families illustrates an increasing, and increasingly productive, integration between theoreticians and empiricists.     

The evolutionary outcome of sexual conflict

Inter-locus sexual conflict occurs by definition when there is sexually antagonistic selection on a trait so that the optimal trait value differs between the sexes. As a result, there is selection on each sex to manipulate the trait towards its own optimum and resist such manipulation by the other sex. Sexual conflict often leads additionally to the evolution of harmful behaviour and to self-reinforcing and even perpetual sexually antagonistic coevolution. In an attempt to understand the determinants of these different outcomes, I compare two groups of traits-those related to parental investment (PI) and to mating-over which there is sexual conflict, but which have to date been explored by largely separate research traditions. A brief review suggests that sexual conflict over PI, particularly over PI per offspring, leads less frequently to the evolution of manipulative behaviour, and rarely to the evolution of harmful behaviour or to the rapid evolutionary changes which may be symptomatic of sexually antagonistic coevolution. The chief determinants of the evolutionary outcome of sexual conflict are the benefits of manipulation and resistance, the costs of manipulation and resistance, and the feasibility of manipulation. All three of these appear to contribute to the differences in the evolutionary outcome of conflicts over PI and mating. A detailed dissection of the evolutionary changes following from sexual conflict exposes greater complexity than a simple adaptation-counter-adaptation cycle and clarifies the role of harm. Not all of the evolutionary changes that follow from sexual conflict are sexually antagonistic, and harm is not necessary for sexually antagonistic coevolution to occur. In particular, whereas selection on the trait over which there is conflict is by definition sexually antagonistic, collateral harm is usually in the interest of neither sex. This creates the opportunity for palliative adaptations which reduce collateral harm. Failure to recognize that such adaptations are in the interest of both sexes can hinder our understanding of the evolutionary outcome of sexual conflict.     

Parent–Offspring Conflict in Primates

Parent–offspring conflict (POC) theory (Trivers, 1974) has stimulated controversy in evolutionary biology and behavioral ecology. The theory has been criticized by some primate behavioral researchers on both conceptual and empirical grounds. First, it has been argued that it would be more advantageous to mothers and offspring to agree over the allocation of parental investment and to cooperate rather than to disagree and engage in conflict. Second, some studies have provided data suggesting that primate mothers and offspring engage in behavioral conflict over the scheduling of their activities rather than parental investment. In reality, parent–offspring interactions are likely to involve both cooperation and conflict, and the hypothesis that mothers and infants squabble over the scheduling of their activities is not incompatible with POC theory. Furthermore, the predictions of POC theory are supported by a number of empirical studies of primates. POC theory has enhanced our understanding of the dynamics of parent–offspring relationships in many animal species, and it is very likely that future studies of primates will continue to benefit from using POC theory as an explanatory framework.     

Asynchronous hatching in the burying beetle,Nicrophorus quadripunctatus,maxmizes parental fitness

Life history theory predicts that natural selection favours parents who balance investment across offspring to maximize fitness. Theoretical studies have shown that the optimal level of parental investment from the offspring's perspective exceeds that of its parents, and the disparity between the two generates evolutionary conflict for the allocation of parental investment. In various species, the offspring hatch asynchronously. The age hierarchy of the offspring usually establishes competitive asymmetries within the brood and determines the allocation of parental investment among offspring. However, it is not clear whether the allocation of parental investment determined by hatching pattern is optimal for parent or offspring. Here, we manipulated the hatching pattern of the burying beetle Nicrophorus quadripunctatus to demonstrate the influence of hatching pattern on the allocation of parental investment. We found that the total weight of a brood was largest in the group that mimicked the natural hatching pattern, with the offspring skewed towards early hatchers. This increases parental fitness. However, hatching patterns with more later hatchers had heavier individual offspring weights, which increases offspring fitness, but this hatching pattern is not observed in the wild. Thus, our study suggests that the natural hatching pattern optimizes parental fitness, rather than offspring fitness.     

Packaging of offspring by nests of the ant,Leptothorax longispinosus: parent-offspring conflict and queen-worker conflict

Models of the packaging of offspring predict that parental fitness is maximized by following a set of rules, including the rule to invest the minimal amount in each offspring. Offspring can maximize their fitness by demanding more resources than the parent is selected to give, leading to parent-offspring conflict over packaging. Social insect nests may also experience queen-worker conflict over packaging. Experiments were conducted, using two populations of the ant Leptothorax longispinosus, in order to determine the role of both parent-offspring conflict and queen-worker conflict in packaging. Parent-offspring conflict over packaging was detected towards males and workers, but not to females. This may be because both parental and offspring fitness are maximized by investing as much in possible in females so both parties benefit by cooperating over packaging of females. Queen-worker conflict over packaging was detected for females, males, and workers. The direction taken by the queen-worker conflict is best explained by asymmetries in genetic relatedness among nestmates.     

Beyond promiscuity: mate-choice commitments in social breeding

Obligate eusociality with distinct caste phenotypes has evolved from strictly monogamous sub-social ancestors in ants, some bees, some wasps and some termites. This implies that no lineage reached the most advanced form of social breeding, unless helpers at the nest gained indirect fitness values via siblings that were identical to direct fitness via offspring. The complete lack of re-mating promiscuity equalizes sex-specific variances in reproductive success. Later, evolutionary developments towards multiple queen-mating retained lifetime commitment between sexual partners, but reduced male variance in reproductive success relative to female''s, similar to the most advanced vertebrate cooperative breeders. Here, I (i) discuss some of the unique and highly peculiar mating system adaptations of eusocial insects; (ii) address ambiguities that remained after earlier reviews and extend the monogamy logic to the evolution of soldier castes; (iii) evaluate the evidence for indirect fitness benefits driving the dynamics of (in)vertebrate cooperative breeding, while emphasizing the fundamental differences between obligate eusociality and cooperative breeding; (iv) infer that lifetime commitment is a major driver towards higher levels of organization in bodies, colonies and mutualisms. I argue that evolutionary informative definitions of social systems that separate direct and indirect fitness benefits facilitate transparency when testing inclusive fitness theory.     

On the assignment of fitness to parents and offspring: whose fitness is it and when does it matter?

There has been a long‐standing conceptual debate over the legitimacy of assigning components of offspring fitness to parents for purposes of evolutionary analysis. The benefits and risks inherent in assigning fitness of offspring to parents have been given primarily as verbal arguments and no explicit theoretical analyses have examined quantitatively how the assignment of fitness can affect evolutionary inferences. Using a simple quantitative genetic model, we contrast the conclusions drawn about how selection acts on a maternal character when components of offspring fitness (such as early survival) are assigned to parents vs. when they are assigned directly to the individual offspring. We find that there are potential shortcomings of both possible assignments of fitness. In general, whenever there is a genetic correlation between the parental and direct effects on offspring fitness, assigning components of offspring fitness to parents yields incorrect dynamical equations and may even lead to incorrect conclusions about the direction of evolution. Assignment of offspring fitness to parents may also produce incorrect estimates of selection whenever environmental variation contributes to variance of the maternal trait. Whereas assignment of offspring fitness to the offspring avoids these potential problems, it introduces the possible problem of missing components of kin selection provided by the mother, which may not be detected in selection analyses. There are also certain conditions where either model can be appropriate because assignment of offspring fitness to parents may yield the same dynamical equations as assigning offspring fitness directly to offspring. We discuss these implications of the alternative assignments of fitness for modelling, selection analysis and experimentation in evolutionary biology.     

The quantitative genetic basis of offspring solicitation and parental response in a passerine bird with biparental care.

The coevolution of parental investment and offspring solicitation is driven by partly different evolutionary interests of genes expressed in parents and their offspring. In species with biparental care, the outcome of this conflict may be influenced by the sexual conflict over parental investment. Models for the resolution of such family conflicts have made so far untested assumptions about genetic variation and covariation in the parental resource provisioning response and the level of offspring solicitation. Using a combination of cross-fostering and begging playback experiments, we show that, in the great tit (Parus major), (i) the begging call intensity of nestlings depends on their common origin, suggesting genetic variation for this begging display, (ii) only mothers respond to begging calls by increased food provisioning, and (iii) the size of the parental response is positively related to the begging call intensity of nestlings in the maternal but not paternal line. This study indicates that genetic covariation, its differential expression in the maternal and paternal lines and/or early environmental and parental effects need to be taken into account when predicting the phenotypic outcome of the conflict over investment between genes expressed in each parent and the offspring.     

The evolution of mate choice and the potential for conflict between species and mate-quality recognition

Understanding how individuals select mates becomes complex when high-quality conspecifics resemble heterospecifics. Individuals facing such a situation may be unable to effectively identify both conspecifics (species recognition) and high-quality mates that can confer fitness benefits to the choosy individual or its offspring (mate-quality recognition). Here I suggest when a conflict may occur between species and mate-quality recognition, discuss the evolutionary consequences stemming from this conflict, and present a model of mate-preference evolution in response to heterospecifics. Determining how species and mate-quality recognition interact to shape mate-choice decisions is important for understanding the diversification of sexually selected traits among closely related taxonomic groups, the use of complex sensory systems for detecting mates, and seemingly inappropriate mate-choice decisions.     

Sex ratio manipulation within broods of house wrens, Troglodytes aedon

Trivers & Willard (1973, Science, 179, 90-92) developed an economic theory of parental investment to explain how the relative profitability of sons and daughters varies under specific ecological conditions. In their maternal condition hypothesis they proposed that in polygynous species, the sex of an offspring should be associated with the amount of parental care likely to be made available to it. In these species, the amount of parental investment directed towards offspring may differentially influence the fitness of male and female offspring because males in better than average condition as adults may enjoy larger fitness gains than a female would if she were in better than average condition, while the reverse may be true when conditions are poor. I tested this hypothesis by determining the sex of specific offspring within house wren broods. Because hatching is asynchronous and fledging is synchronous in this polygynous species, last-hatched young fledge having received less parental care than their broodmates. I predicted that last-hatched offspring would be more likely to be female. I found that these young were indeed more likely to be females, were more likely to have hatched from last-laid eggs and were fledging in poor condition relative to their broodmates. I propose that female house wrens behave in a manner consistent with the predictions of the Trivers & Willard hypothesis by producing female offspring last in the laying sequence of their clutches. Copyright 2000 The Association for the Study of Animal Behaviour.     

Selection for increased allocation to offspring number under environmental unpredictability

According to life-history theory, the evolution of offspring size is constrained by the trade-off between allocation of resources to individual offspring and the number of offspring produced. Existing models explore the ecological consequences of offspring size, whereas number is invariably treated simply as an outcome of the trade-off with size. Here I ask whether there is a direct evolutionary advantage of increased allocation to offspring number under environmental unpredictability. Variable environments are expected to select for diversification in the timing of egg hatch and seed germination, yet the dependence of the expression of diversification strategies, and thus parental fitness, on offspring number has not previously been recognized. I begin by showing that well-established sampling theory predicts that a target bethedging diversification strategy is more reliably achieved as offspring number increases. I then use a simulation model to demonstrate that higher offspring number leads to greater geometric mean fitness under environmental uncertainty. Natural selection is thus expected to act directly to increase offspring number under assumptions of environmental unpredictability in season quality.     

Direct benefits of choosing a high‐fitness mate can offset the indirect costs associated with intralocus sexual conflict

Intralocus sexual conflict generates a cost to mate choice: high‐fitness partners transmit genetic variation that confers lower fitness to offspring of the opposite sex. Our earlier work in the fruit fly, Drosophila melanogaster, revealed that these indirect genetic costs were sufficient to reverse potential “good genes” benefits of sexual selection. However, mate choice can also confer direct fitness benefits by inducing larger numbers of progeny. Here, we consider whether direct benefits through enhanced fertility could offset the costs associated with intralocus sexual conflict in D. melanogaster. Using hemiclonal analysis, we found that females mated to high‐fitness males produced 11% more offspring compared to those mated to low‐fitness males, and high‐fitness females produced 34% more offspring than low‐fitness females. These direct benefits more than offset the reduction in offspring fitness caused by intralocus sexual conflict, creating a net fitness benefit for each sex to pairing with a high‐fitness partner. Our findings highlight the need to consider both direct and indirect effects when investigating the fitness impacts of mate choice. Direct fitness benefits may shelter sexually antagonistic alleles from selection, suggesting a novel mechanism for the maintenance of fitness variation.     

Decision-making in variable environments-- a case of group selection and inter-generational conflict?

Suppose organisms need to engage in a particular action exactly once during some fixed period of time. Further suppose they can time this action to optimise their fitness based on the expected current payoff and the probability distribution of later payoffs. For an example we consider the timing of the annual nuptial flight in eusocial insects. Using two population genetics models, we ask whether stochasticity leads to evolutionary conflict between the queen and her offspring. We find that the winning phenotype is independent of who controls the timing. The best response to any non-equilibrium population strategy is the same in both control scenarios, a result that carries over to the diploid case. Although inter-generational conflict is therefore ruled out, the models support a previous observation that at equilibrium some of the offspring have a lower expected payoff than others. By measuring fitness in terms of relative reproductive success, we show that all individuals are in fact equally well off making group-selectionist arguments unnecessary. As such, the models should improve our understanding of the difficult conceptual problem of the unit of natural selection in stochastic environments.     

Living with relatives: lessons from avian family systems*

Family-dwelling birds provide excellent opportunities for testing evolutionary predictions about social interactions among relatives. Their combination of behavioural complexity with cultural simplicity makes them ideal model systems in which to search for fundamental biological rules of social interaction. In this plenary, I provide a personalized overview of current thinking about both the evolution of families and the social dynamics to be expected among family members. Using an adaptationist/economic approach that uses fitness as its currency, I develop a set of 15 predictions about family formation, family stability, familial cooperation, familial competition and conflict resolution among kin. I argue that knowledge of four basic parameters, genetic relatedness, social dominance, the benefits of group living and the probable success of independent reproduction, can explain many aspects of family life in birds. I further suggest that this evolutionary perspective is generalizable across taxa and will provide new insights into understanding animal family systems in other species, including our own.     

Direct fitness correlates and thermal consequences of facultative aggregation in a desert lizard

Social aggregation is a common behavioral phenomenon thought to evolve through adaptive benefits to group living. Comparing fitness differences between aggregated and solitary individuals in nature - necessary to infer an evolutionary benefit to living in groups - has proven difficult because communally-living species tend to be obligately social and behaviorally complex. However, these differences and the mechanisms driving them are critical to understanding how solitary individuals transition to group living, as well as how and why nascent social systems change over time. Here we demonstrate that facultative aggregation in a reptile (the Desert Night Lizard, Xantusia vigilis) confers direct reproductive success and survival advantages and that thermal benefits of winter huddling disproportionately benefit small juveniles, which can favor delayed dispersal of offspring and the formation of kin groups. Using climate projection models, however, we estimate that future aggregation in night lizards could decline more than 50% due to warmer temperatures. Our results support the theory that transitions to group living arise from direct benefits to social individuals and offer a clear mechanism for the origin of kin groups through juvenile philopatry. The temperature dependence of aggregation in this and other taxa suggests that environmental variation may be a powerful but underappreciated force in the rapid transition between social and solitary behavior.     

Darwinism without populations: a more inclusive understanding of the "Survival of the Fittest"

Following Wallace's suggestion, Darwin framed his theory using Spencer's expression "survival of the fittest". Since then, fitness occupies a significant place in the conventional understanding of Darwinism, even though the explicit meaning of the term 'fitness' is rarely stated. In this paper I examine some of the different roles that fitness has played in the development of the theory. Whereas the meaning of fitness was originally understood in ecological terms, it took a statistical turn in terms of reproductive success throughout the 20th Century. This has lead to the ever-increasing importance of sexually reproducing organisms and the populations they compose in evolutionary explanations. I will argue that, moving forward, evolutionary theory should look back at its ecological roots in order to be more inclusive in the type of systems it examines. Many biological systems (e.g. clonal species, colonial species, multi-species communities) can only be satisfactorily accounted for by offering a non-reproductive account of fitness. This argument will be made by examining biological systems with very small or transient population structures. I argue this has significant consequences for how we define Darwinism, increasing the significance of survival (or persistence) over that of reproduction.     

Intralocus sexual conflict,adaptive sex allocation,and the heritability of fitness

Intralocus sexual conflict arises when selection favours alternative fitness optima in males and females. Unresolved conflict can create negative between‐sex genetic correlations for fitness, such that high‐fitness parents produce high‐fitness progeny of their same sex, but low‐fitness progeny of the opposite sex. This cost of sexual conflict could be mitigated if high‐fitness parents bias sex allocation to produce more offspring of their same sex. Previous studies of the brown anole lizard (Anolis sagrei) show that viability selection on body size is sexually antagonistic, favouring large males and smaller females. However, sexual conflict over body size may be partially mitigated by adaptive sex allocation: large males sire more sons than daughters, whereas small males sire more daughters than sons. We explored the evolutionary implications of these phenomena by assessing the additive genetic (co)variance of fitness within and between sexes in a wild population. We measured two components of fitness: viability of adults over the breeding season, and the number of their progeny that survived to sexual maturity, which includes components of parental reproductive success and offspring viability (RS^V). Viability of parents was not correlated with adult viability of their sons or daughters. RS^V was positively correlated between sires and their offspring, but not between dams and their offspring. Neither component of fitness was significantly heritable, and neither exhibited negative between‐sex genetic correlations that would indicate unresolved sexual conflict. Rather, our results are more consistent with predictions regarding adaptive sex allocation in that, as the number of sons produced by a sire increased, the adult viability of his male progeny increased.     

Parental antagonism and parent-offspring co-adaptation interact to shape family life

The family is an arena for conflicts between offspring, mothers and fathers that need resolving to promote the evolution of parental care and the maintenance of family life. Co-adaptation is known to contribute to the resolution of parent-offspring conflict over parental care by selecting for combinations of offspring demand and parental supply that match to maximize the fitness of family members. However, multiple paternity and differences in the level of care provided by mothers and fathers can generate antagonistic selection on offspring demand (mediated, for example, by genomic imprinting) and possibly hamper co-adaptation. While parent-offspring co-adaptation and parental antagonism are commonly considered two major processes in the evolution of family life, their co-occurrence and the evolutionary consequences of their joint action are poorly understood. Here, we demonstrate the simultaneous and entangled effects of these two processes on outcomes of family interactions, using a series of breeding experiments in the European earwig, Forficula auricularia, an insect species with uniparental female care. As predicted from parental antagonism, we show that paternally inherited effects expressed in offspring influence both maternal care and maternal investment in future reproduction. However, and as expected from the entangled effects of parental antagonism and co-adaptation, these effects critically depended on postnatal interactions with caring females and maternally inherited effects expressed in offspring. Our results demonstrate that parent-offspring co-adaptation and parental antagonism are entangled key drivers in the evolution of family life that cannot be fully understood in isolation.