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.     

Costly Solicitation, Timing of Offspring Conflict, and Resource Allocation in Plants

The theory of parent–offspring conflict is extended toplants that produce many offspring in one reproductive event.The energetic cost of begging signals and the timing of offspringconflict are explicitly taken into account. We find that ifthe indirect costs of increased provisioning of selfish offspringare borne by their brood mates, then offspring are selectedto solicit in so costly a way that a substantial part of parentalinvestment in a brood goes to solicitation rather than offspring'sgrowth and survival. Consequently, offspring conflict oftenresults in smaller seed size than the parental optimum in theabsence of conflict, although each offspring still consumesmore resources than the amount its mother is willing to give.While the optimal sex allocation can be shown to be independentof solicitation and sibling conflict, the overall reproductiveeffort is always lowered by parent–offspring conflict.The timing of offspring conflict during the period of parentalinvestment is demonstrated to be an important factor that influencesthe outcome of parent–offspring conflict. The more resourcesare allocated to individual offspring before the occurrenceof offspring solicitation, the less offspring should solicit,and hence the closer the offspring size to the parental optimum.Copyright 2000 Annals of Botany Company Evolutionarily stable strategy, parent–offspring conflict, parental investment, reproductive resource allocation, seed size, solicitation, timing of offspring conflict     

Shared and unshared parental investment,parent-offspring conflict and brood size

Taking as our starting point Trivers' (1974) account of parent-offspring conflict, we develop models of the influence of brood size on the optimal level of parental investment (PI) in the whole brood for parent and offspring, and on the magnitude of conflict between them. A modification of Trivers' model is proposed. In general, the benefit of an act of PI to an offspring in a brood of size N is (N+1)/N times the benefit to its parent. Therefore as brood size increases, offspring benefit approaches parental benefit, and this is because an increasing proportion of the offspring's benefit is being gained through siblings, to which offspring and parent are equally related. A distinction is drawn between ‘shared’ and ‘unshared’ types of PI. When PI is shared the total benefit accruing is not directly gained by all offspring but is shared amongst them (e.g. food brought to the young). In contrast, unshared PI can simultaneously benefit some or all of the brood (e.g. types of anti-predator defence). For shared investment, PI and conflict are predicted to increase with brood size. Two models of unshared anti-predator defence are described. If the predator characteristically takes the whole brood when it strikes (e.g. altricial nestlings) PI is predicted to increase and conflict decline with brood size, although this effect is inhibited or even reversed for high risk defence tactics because of the higher cost to larger broods if the parent dies. When the predator takes a single offspring (e.g. precocial birds) the parent's optimum PI is independent of brood size, the offspring's optimum PI declines in larger broods and conflict again declines with brood size. The parent is commonly expected to win the conflict over anti-predator care. Predictions concerning PI levels gain support from existing data, largely for birds, but evaluation of those for conflict must await the collection of new data. The distinction between shared and unshared investment is applicable to altruistic behaviour in general.     

Parent-offspring conflict over clutch size

Summary We present a model for sexually-reproducing diploids in which a female can produce a variable (generally large) clutch size, where the sibs then compete over some fixed resource, and where certain offspring use siblicide to reduce the primary clutch/brood size created by the mother. Where siblicide involves neither direct energy loss (e.g. fighting cost) nor gain (e.g. cannibalism) to an offspring, the optimal clutch size for an offspring can differ from the optimum for the mother, i.e. there can be parent-offspring conflict over clutch size. The magnitude of this evolutionary conflict (measured in terms of difference between clutch size optima) increases with multipaternity of the brood and with the steepness of the initial decline in offspring survivorship (through sib-competition as further offspring are added to the brood). However, the disparity in clutch size optima may not be great. Where the integer clutch size optima are the same, there will clearly be no conflict. Where this differs, resolution of the evolutionary conflict could involve much apparent behavioral conflict, commonly manifest as siblicidal aggression.The ESS (evolutionarily stable strategy) for such a game will depend upon the direct costs and benefits of siblicide, as well as on the indirect costs to sibs via relatedness. If the only costs of siblicide arise through relatedness, then offspring will win in the sense that the eventual clutch size will match the offspring optimum. Whether or not the mother will produce this clutch size depends on the mechanism controlling siblicide. A siblicidal ESS will occur when offspring are programmed to kill a fixed number/proportion of a brood (victim-based siblicide), but not if programmed to reduce the sibship to the offspring optimum (survivor-based siblicide). With survivor-based siblicide, the mother can do no better than to lay the offsprings' optimal clutch size.     

Parent-offspring conflict and the coordination of siblings in gulls

Offspring solicit food from their parents by begging behaviours. Studies on birds suggest that these displays are 'honest signals of need' and adults provide food according to the begging level. However, siblings may compete for parental resources and the begging intensity is expected to change with brood size. Here, we show that in the black-headed gull (Larus ridibundus) an increase of the numbers of siblings can result in a decrease of individual begging cost through nestlings' synchronized signalling. This is in accordance with some mathematical models. As parents respond to the total solicitation emerging from the nest, the probability to get food increases with the number of chicks begging together. The more siblings there are, the more they coordinate their begging while decreasing the number of individual begging bouts. Intra-brood synchronization of begging enables chicks to reduce their effort and hence exerting an important role in parental-offspring negotiation.     

Models of parent-offspring conflict. I. Monogamy

Theoretical models for Trivers (1974) concept of parent-offspring conflict are examined for species in which the effects of the conflict are felt by full sibs. A rare conflictor gene will spread if (f(m) greater than 1/2(m + 1), where f(m) is the fitness gained by a conflictor relative to a non-conflictor offspring (f(m) greater than 1), and m is the amount of parental investment taken by a conflictor relative to m = 1 for a non-conflictor. The range of m alleles which can spread against the parent optimum decreases as the cost to the parent increases until a point is reached where there is no conflict of evolutionary interests. There would be no polymorphism for conflictor: non-conflictor alleles unless special conditions prevail. The conflictor allele which spreads most rapidly as a rare mutant against the parental optimum is not an evolutionarily stable strategy (ESS). The ESS for parent-offspring conflict in monogamous species has mo = f(mo)/2[df(mo)/dmo]. The analytical solutions are confirmed throughout by simulations.     

Error-related negativity predicts reinforcement learning and conflict biases

The error-related negativity (ERN) is an electrophysiological marker thought to reflect changes in dopamine when participants make errors in cognitive tasks. Our computational model further predicts that larger ERNs should be associated with better learning to avoid maladaptive responses. Here we show that participants who avoided negative events had larger ERNs than those who were biased to learn more from positive outcomes. We also tested for effects of response conflict on ERN magnitude. While there was no overall effect of conflict, positive learners had larger ERNs when having to choose among two good options (win/win decisions) compared with two bad options (lose/lose decisions), whereas negative learners exhibited the opposite pattern. These results demonstrate that the ERN predicts the degree to which participants are biased to learn more from their mistakes than their correct choices and clarify the extent to which it indexes decision conflict.     

Colony size,social complexity and reproductive conflict in social insects

The broad limits of mature colony size in social insect species are likely to be set by ecological factors. However, any change in colony size has a number of important social consequences. The most fundamental is a change in the expected reproductive potential of workers. If colony size rises, workers experience a fall in their chances of becoming replacement reproductives and, it is shown, increasing selection for mutual inhibition of one another's reproduction (worker policing). As workers’ reproductive potential falls, the degree of dimorphism between reproductive and worker castes (morphological skew) can rise. This helps explain why small societies have low morphological skew and tend to be simple in organization, whereas large societies have high morphological skew and tend to be complex. The social consequences of change in colony size may also alter colony size itself in a process of positive feedback. For these reasons, small societies should be characterized by intense, direct conflict over reproduction and caste determination. By contrast, conflict in large societies should predominantly be over brood composition, and members of these societies should be relatively compliant to manipulation of their caste. Colony size therefore deserves fuller recognition as a key determinant, along with kin structure, of social complexity, the reproductive potential of helpers, the degree of caste differentiation, and the nature of within-group conflict.     

Models of parent-offspring conflict. V. Effects of the behaviour of the two parents

In the absence of any parent-offspring conflict, the total parental investment per offspring should be less when two parents collaborate in caring for the offspring than when only one parent invests. This does not necessarily mean that offspring fare less well when both parents invest. The ‘ideal’ amount of parental investment for an offspring to take is always greater than is ‘ideal’ for the parent to allocate (Trivers 1974). The offspring's optimum is higher if the offspring's action affects the reproductive success of only one parent and lower if both parents are affected (e.g. two-parent investment, or lifelong monogamy). The difference between the parental optimum and the offspring optimum depends on the mating system and on the form of conflict (between successive broods, or within broods), and prescribes a ‘conflict range’. The extent of conflict cannot be deduced solely from a knowledge of the average relatedness between siblings. The conflict is likely to be resolved by an ESS in which intermediate (compromise) levels of investment are paid out to offspring, which nevertheless continue to make costly demands for yet more investment. The degree of conflict can be measured by the extent to which offspring subject their parents to aggressive demands for extra investment, and is likely to be greater when two parents collaborate equally over investment than when only one parent invests. When only one parent invests, conflict is higher if sibling-competition is between siblings in the same broods (intra-brood) than when it is between progeny in successive broods (inter-brood). However, the reverse will tend to be the case when both parents invest equally.     

A kin-selection approach to the resolution of sex-ratio conflict between mates

We investigate an instance of conflict between mates over the sex ratio of their brood. We construct a kin-selection model for the evolution of the sex ratio assuming local resource competition (LRC) among females. We explore two basic scenarios: (a) the case where parents make simultaneous sex-ratio decisions (the simultaneous allocation model); and (b) the case where parental sex-ratio decisions occur one after the other (the sequential allocation model). In the simultaneous investment model, resolution of the conflict between mates depends on the extent to which relative paternal contribution influences the brood sex ratio. In the sequential allocation model, fathers determine primary sex-ratio through fertilization bias; then mothers modify the paternal sex-ratio decision by adjusting the level of investment of some resource that contributes to offspring survival. Under the sequential model, a compromise is always achieved; however this compromise favours one perspective or the other, depending on the extent to which maternal investment influences offspring survival.     

An asymmetric parental investment conflict with continuous strategy sets

In the parental investment conflict each of the sexes decides how much to invest in its brood, where its decision influences both sexes' fitness. In nature, each species is usually characterized by a common parental care pattern, male-only care, female-only care or biparental care. A possible way for understanding the factors that have led each species to adopt its unique parental care pattern is to analyse a male's and a female's decision process using a game-theoretical model. This paper suggests a two-stage game-theoretical model with two types of players, male and female. During the game each parent makes three decisions. The interval between the beginning of the game, i.e. after mating and having offspring, and the moment a parent starts to care for them is a random variable. Thus, in the first stage a parent chooses the cumulative probability distribution of this interval, and its amount of parental care. In the second stage the other parent chooses its probability for cooperation. It is assumed that as long as parental care is not provided the offspring are at risk, and that parental caring accrues a different cost for each sex. We compute the Evolutionary Stable Strategies (ESS) under payoff-relevant asymmetry, and show that uniparental and biparental care are possible ESS. We also characterize cases where the sex having the lower cost "forces" the sex having the higher cost to care and vice versa.     

Sexual conflict and parental care in magnificent frigatebirds: full compensation by deserted females

Parental care is a cooperative venture between a male and a female in many socially monogamous birds. Care is costly, and thus, sexual conflict arises between the parents about how much effort they should invest into rearing their young. The sexual conflict over care is most apparent when one parent abandons the brood before the offspring are independent. The deserted parent has three options: (1) desert the brood because a single parent is unable to raise the young on its own; (2) continue care provision at the same level as during biparental care, and thus do not compensate for the absence of mate; or (3) increase care and compensate partially or totally. We investigated these options in the magnificent frigatebird, Fregata magnificens, a species in which the male deserts his mate and brood before the chick is independent. During biparental care, females fed the chick more often than the males. After their mate deserted, the females nearly doubled their feeding rate and thus, fully compensated for the lost care. Consistent with these observations, growth rates of chicks provided with biparental and female-only care did not differ. These results support recent theoretical models of parental care, and suggest that females may withhold care during biparental care to manoeuvre their mates into prolonged care provision. A female only provides at her full capacity once her mate has deserted.     

Sibling competition stabilizes signalling resolution models of parent-offspring conflict

Young of altricial birds use conspicuous displays to solicit food from their parents. There is experimental evidence that the intensity of these displays is correlated with the level of food deprivation of young, and that parents respond to increased levels of solicitation by increasing the rate of food delivery to the nest. Game-theoretical models based on the handicap principle show that, when solicitation is costly, there is a signalling equilibrium at which there is a one-to-one correspondence between the condition of the young and the intensity of their display. Parents use this information to adjust their levels of investment on the current offspring. However, the models also have a non-signalling equilibrium, and computer simulations show that only the non-signalling equilibrium is stable. Here I show that when direct sibling competition is introduced into the model, in such a way that parents have control on the amount of food provided to the nest, but not on the way the food is allocated among siblings, the non-signalling equilibrium disappears and the signalling equilibrium becomes stable.     

EVOLUTION OF OBLIGATE SIBLICIDE IN BOOBIES. 2: FOOD LIMITATION AND PARENT–OFFSPRING CONFLICT

Proximate limitation on parental food delivery has long been invoked to explain the evolution of single-chick broods of pelagic seabirds such as masked boobies (Sula dactylatra). A second possible proximate limit on brood size is siblicide driven by genetic parent–offspring conflict (POC) over brood size, if siblicidal offspring can reduce brood size to one even if the parents' optimal brood size is greater than one. I tested these two hypotheses by experimentally suppressing obligate siblicide in masked booby broods and comparing breeding parameters of these broods with unmanipulated single-chick control broods. Per capita mortality rate of experimental nestlings was higher than that of controls, but this deficit was more than made up by larger brood size. Parents of experimental broods brought more food to offspring, had higher fledging success, and apparently incurred no additional major short-term cost of reproduction, relative to parents of control broods, thus refuting the food limitation hypothesis. Estimates of inclusive fitness of chicks in experimental broods were higher than were those of control nestlings, a result inconsistent with the POC hypothesis that the siblicidal offspring's optimal brood size is one while the parents' optimum is greater than one. This discrepency between natural brood size and apparent brood size optima might be resolved in several ways: experimental artifacts may give misleading estimates of optimal brood size; experimental and control offspring may have different reproductive values at the time of fledging; nestling masked boobies may face a special frequency-dependent case of POC in which the high risk of sharing a nest with a siblicidal sibling makes invasion of other behavioral genotypes difficult even when offspring and parent inclusive fitnesses are higher from a nonsiblicidal brood of two than from a brood of one.     

Models of parent-offspring conflict. II. Promiscuity

The population genetics of Trivers (1974) concept of parent-offspring is examined for species in which the effects of the conflict are felt by future half-sibs, as in promiscuous mating systems in which the male shows no parental care. Whether or not a rare conflictor gene will spread in a non-conflictor population depends on f(m) greater than (m + 1)/(0.5m + 1.5) for a dominant gene, and on f(m) greater than 1/4(7 + 3) for a recessive gene; f(m) is the fitness gained by a conflictor relative to a non-conflictor offspring [f(m) greater than 1], and m is the amount of parental investment taken by a conflictor relative to m = 1 for a non-conflictor. The ESS value for conflict (mo) in promiscuous species with zero male parental care has mo = f(mo)/4[df(mo)/dmo]. However, where the male maintains the same harem for several breeding seasons, or where there is promiscuity but both sexes contribute equally to parental care, conditions for conflict are equivalent to monogamy.     

Cooperation, conflict, and crèching behavior in goldeneye ducks

Crèching behavior, or brood amalgamation, results in offspring being reared by adults other than their genetic parents. Although a variety of hypotheses have been proposed to explain this behavior, most assume either that brood amalgamation is accidental (i.e., nonselected) or that adoption of young is selected for because of social benefits to the young and/or adopting parents. We propose, instead, that brood amalgamation is a function of two separate processes: brood desertion and brood adoption. To examine brood desertion, we develop a graphic model to predict when parents should abandon their young and we test this model experimentally for the Barrow's goldeneye (Bucephala islandica). As predicted, females deserted their offspring when the size of the brood was experimentally reduced. Brood adoption occurred when deserted ducklings joined other broods. However, the success of ducklings in doing so was strongly dependent on the availability of potential host broods and on the age of the recipient broods. Foreign ducklings were readily accepted into young broods (<10 d old) but invariably were rejected from old broods. We could detect no benefits or costs of brood adoption to the host females, contrary to the expectations of a social benefit hypothesis. Our experiments indicate that Crèching behavior is driven by selection on adults to abandon their brood when the benefits of continued investment are outweighed by the reduction in future reproduction and selection on deserted ducklings to join other broods to obtain parental care. Rather than a form of cooperative brood care, Crèching in goldeneyes is perhaps best considered as a form of reproductive parasitism, entailing parent-offspring conflict over brood desertion and intergenerational conflict over adoption of abandoned young.     

Reproductive consequences of population divergence through sexual conflict

Sexual-selection research increasingly focuses on reproductive conflicts between the sexes. Sexual conflict, divergent evolutionary interests of males and females, can cause rapid antagonistic coevolution of reproductive traits and is a potentially powerful speciation engine. This idea has theoretical and comparative support but remains controversial. Recent experimental evidence from Sepsis cynipsea indicates that populations with greater sexual conflict diverged more quickly; females were less likely to mate with males from other populations when flies had evolved under high levels of sexual conflict. The consequences of this divergence have not been addressed, so here we assess two female fitness surrogates after 44 generations of evolving (and diverging) under three different levels of sexual conflict. Longevity after copulation was negatively associated with the degree of sexual conflict under which flies evolved, and housing females with males also reduced female longevity. Female lifetime reproductive success (LRS) also tended to decrease with increasing conflict. However, there was evidence of either sexual-selection fitness benefits at intermediate levels of sexual selection and conflict or inbreeding depression in the smallest populations (those with the lowest levels of conflict). Nevertheless, the results indicate that there can be a fitness load associated with sexual selection and support claims that sexual conflict can lead to reproductive isolation.     

How costly is the honest signaling of need?

ESS models of biological signaling have shown that costly signals can provide honest information. In the context of parent-offspring conflict over the allocation of resources by parents to their young, the theory explains costly offspring solicitation behavior as an accurate signal of offspring need to parents who cannot assess offspring condition directly. In this paper, we provide a simple but general characterization of the honest signaling of need in models of parent-offspring conflict: the offspring's signaling cost is proportional to the parent's fitness loss from satisfying the offspring's resource requirement. The factor of proportionality is given by a measure of the extent of parent-offspring conflict that depends only on coefficients of relatedness. These results hold for interbrood conflict with uniparental investment even if the relationship between offspring condition and resource requirement is not monotonic, and extend to cases of biparental care, uncertainty concerning the parent's condition, and intra-brood conflict. Copyright 1999 Academic Press.     

Parent-offspring conflict: A case of arrested development

The theory of parent-offspring conflict (POC) provides a plausible evolutionary foundation for the dissonant behavioral interactions commonly observed between adults and their progeny. It has been modelled extensively, but its predictions for phenotypes are murky and have been subjected to scant empirical testing. The least ambiguous cases are likely to involve taxa where offspring exert real power. Recent experimental work indicates that worker bees manipulate brood sex ratios differently from the queen. By contrast, most studies of avian brood reduction and mammalian ‘weaning conflict’ remain open to multiple interpretations. In general, POC may owe its current hegemony to the paucity of alternative explanations for parent-offspring squabbles. Reassessments of basic assumptions about what both parties ‘really want’ need to be linked to experimentation, field-oriented modelling and pluralism for this provocative theory to become broadly useful.     

Sexual conflict and speciation.

We review the significance of two forms of sexual conflict (different evolutionary interests of the two sexes) for genetic differentiation of populations and the evolution of reproductive isolation. Conflicting selection on the alleles at a single locus can occur in males and females if the sexes have different optima for a trait, and there are pleiotropic genetic correlations between the sexes for it. There will then be selection for sex limitation and hence sexual dimorphism. This sex limitation could break down in hybrids and reduce their fitness. Pleiotropic genetic correlations between the sexes could also affect the likelihood of mating in interpopulation encounters. Conflict can also occur between (sex-limited) loci that determine behaviour in males and those that determine behaviour in females. Reproductive isolation may occur by rapid coevolution of male trait and female mating preference. This would tend to generate assortative mating on secondary contact, hence promoting speciation. Sexual conflict resulting from sensory exploitation, polyspermy and the cost of mating could result in high levels of interpopulation mating. If females evolve resistance to make pre- and postmating manipulation, males from one population could be more successful with females from the other, because females would have evolved resistance to their own (but not to the allopatric) males. Between-locus sexual conflict could also occur as a result of conflict between males and females of different populations over the production of unfit hybrids. We develop models which show that females are in general selected to resist such matings and males to persist, and this could have a bearing on both the initial level of interpopulation matings and the likelihood that reinforcement will occur. In effect, selection on males usually acts to promote gene flow and to restrict premating isolation, whereas selection on females usually acts in the reverse direction. We review theoretical models relevant to resolution of this conflict. The winning role depends on a balance between the ''value of winning'' and ''power'' (relating to contest or armament costs): the winning role is likely to correlate with high value of winning and low costs. Sperm-ovum (or sperm-female tract) conflicts (and their plant parallels) are likely to obey the same principles. Males may typically have higher values of winning, but it is difficult to quantify ''power'', and females may often be able to resist mating more cheaply than males can force it. We tentatively predict that sexual conflict will typically result in a higher rate of speciation in ''female-win'' clades, that females will be responsible for premating isolation through reinforcement, and that ''female-win'' populations will be less genetically diverse.