The Princeton Guide to Evolution

VII.8

Evolution of Parental Care

Mathias Kölliker, Per T. Smiseth, and Nick J. Royle

OUTLINE

1. Natural diversity in forms of parental care

2. Origin and evolution of parental care

3. Evolutionary maintenance of parental care

4. Genetics and epigenetics of parental care

5. Sociality beyond family

Across the animal kingdom there are many species in which parents enhance their offspring’s fitness by providing various forms of care. In some animal taxa, such as birds and mammals, almost all species have parental care, and parental care is complex and necessary for offspring survival. In other taxa, such as fish, reptiles, amphibians, or invertebrates, parental care occurs more sporadically, is more variable, is often less complex, and is not always obligate. The diversity in the forms of parental care is vast, ranging from the choice of oviposition sites to providing food, shelter, and protection to the young (table 1). These different forms of care are adaptations to one or more ecological challenges and form part of an animal’s life history and reproductive strategy. The ecology and life history of a species determine the benefits and costs associated with parental care and, hence, the likelihood that care evolves and is maintained. Evolutionary conflicts between parents and offspring, among siblings, and between male and female parents underlie the evolutionary maintenance of parental care. These conflicts generate novel selection pressures on parental care: how much is provided, who provides it, and how it is allocated among offspring. The evolution of parental care is a coevolutionary process because parental and offspring fitness is determined not only by their respective phenotypic and genotypic characteristics but also by the way in which parents and offspring interact with one another. As a result, evolutionary trajectories of parental care traits can be diverse and complex and play an important role in the evolution of other forms of social behavior, such as eusociality.

GLOSSARY

Correlational Selection. Selection favoring particular combinations of parent and offspring traits rather than individual traits in isolation.

Inclusive Fitness. An individual’s own fitness measured through its own survival and reproduction (direct fitness) in addition to the survival and reproduction of related individuals weighed by genetic relatedness (indirect fitness).

Parental Care. Any parental trait—behavioral or other—that increases the fitness of a parent’s offspring and that is likely to have originated and/or is currently maintained for this function. Measurement: parental behavior/phenotype.

Parental Effect. The causal effects that the parent’s phenotype has on the offspring’s phenotype, including its growth and survival, over and above direct effects due to genes inherited from parents. Measurement: change in offspring phenotype due to parental care.

Parental Effort. The combined fitness costs—in terms of reduced mating effort and/or somatic effort—that parents incur owing to the production and care of all offspring in a given biologically relevant period, such as a breeding attempt; ultimate measure of cost. Measurement: reduction in mating and/or survival prospects due to parental care.

Parental Expenditure. The expenditure of parental resources on parental care of one or more offspring; proximate measure of cost. Measurement: time, energy, food spent on parental care.

Parental Investment. Any investment by the parent in an individual offspring that increases the offspring’s chance of survival (i.e., offspring fitness) at the cost of the parent’s ability to invest in other offspring (Trivers 1972).

Parent-Offspring Coadaptation. The coevolutionary process and outcome of adaptation by parents to variation in offspring traits, and adaptation by offspring to variation in parental care.

Parent-Offspring Conflict. The difference between the optima for parental investment (in terms of inclusive fitness) from the perspective of a gene expressed in the caring parent and a gene expressed in its offspring. Offspring are usually selected to demand more resources than the parent should provide.

Parental care is of interest in evolutionary biology because it is a prime example of an altruistic trait; that is, the recipients of care (offspring) gain a fitness benefit, while the donors (parents) pay an evolutionary cost. Understanding the circumstances under which this occurs is the key to explaining the origins and diversity of forms of care, and sociality. However, although parental care involves altruistic behavior toward offspring, there is also scope for conflict. Asymmetries in relatedness among family members lead to genetic conflicts over the amount and duration of parental care. Furthermore, the genetic bases of traits expressed in families are complex owing to the transgenerational effects on phenotypic expression and the coevolutionary dynamics of parental and offspring traits. This means that parental care is not just a target for selection but generates novel genetic and phenotypic variation that can contribute to the evolution of more complex forms of sociality, such as eusociality (see chapters VII.9, VII.10, and VII.13).

1. NATURAL DIVERSITY IN FORMS OF PARENTAL CARE

Parental care is traditionally studied in animals displaying conspicuous and highly elaborate forms of care, such as bird species where both parents undertake hundreds of foraging trips a day to feed their offspring; or in mammals, where females feed their offspring with highly nutritious and metabolically costly milk. These forms of care are evolutionarily derived and the norm only among birds and mammals. Nevertheless, elaborate parental care is not confined to mammals and birds. Clutton-Brock (1991) provided one of the first comprehensive compilations that detail the diversity of forms and taxonomic distribution of care. For example, various reptiles, fish, insects, arachnids, mollusks, brachiopods, and bryozoans nourish developing embryos via a placenta-like structure similar to that found in mammals, and there are even a small number of amphibians, fish, insects, arachnids, crustaceans, and leeches among which parents provide food for their offspring after hatching or birth, as in birds. Simpler forms of care are more widespread across the animal kingdom, and research on such basal forms of parental care provides important insights into the evolutionary origins of, and later modifications to, parental care. Relatively simple forms of parental care continue to be discovered, as illustrated by recent reports of a deepwater squid (Gonatus onyx) whose females tend their egg mass by holding it in their tentacles, and a caecilian amphibian (Boulengerula taitanus) whose offspring feed by peeling off and eating the outer layers of their mother’s nutrient-rich skin.

There is a vast natural diversity in the forms of care provided by parents that enhance offspring fitness (table 1). These forms of care can be understood as adaptations for dealing with one or more ecological hazards, such as predation, parasites, and food shortages. The most basal and widespread form of care is the provisioning of gametes (eggs) with extra nutrients, such as proteins and lipids, beyond the minimum required for successful fertilization. By definition, this form of care is provided by females, as females are defined as the sex producing the larger gametes. Nevertheless, males of some species may contribute to gamete provisioning by offering nuptial gifts to females. Oviposition- and nest-site selection, as well as nest building, count as parental care provided this behavior enhances the fitness of offspring (usually survival) rather than that of the parent (the parent’s fecundity). The construction of nests and burrows is a widespread form of care in both vertebrates and invertebrates. Nests and burrows provide protection from predators or infanticidal conspecifics but also promotes interactions between parents and offspring owing to spatial aggregation, which is an important factor in the evolution of parental care (see further discussion). More advanced forms of parental care include attendance of eggs or offspring, and food provisioning. Egg or offspring attendance/brooding are very diverse forms of care that include remaining with eggs or offspring in a fixed location for protection against natural enemies, or carriage of eggs or offspring by parents. The various forms whereby parents provide food to their young, whether in the form of mass provisioning of food prior to hatching or progressive provisioning of food after hatching, represent some of the most highly derived forms of care.

Table 1. The main forms of parental care

Form of parental care	Definition and taxonomic distribution
Provisioning of gametes	Eggs are provided with yolk proteins and lipids beyond the minimum required for successful fertilization; in virtually all animal groups, including birds, reptiles, amphibians, spiders or insects, and other invertebrates; to a lesser extent in mammals.
Oviposition- and nest-site selection	Parents choose sites with a suitable microclimate for offspring development/survival and/or that is safe from predation; in virtually all animal groups, including birds, mammals, and insects.
Burrowing and nest building	Cavities are burrowed in a substrate (e.g., soil, wood); many insects, fish, some mammals, reptiles, and birds. A nest is built from materials found in the environment, such as mud and plant materials, from processed plant materials, such as paper or materials produced by the parents themselves, such as silk and mucus; many birds and mammals, and some amphibians, fish, spiders, and insects.
Egg attendance	Parents remain with the eggs at a fixed location after oviposition, usually the oviposition site and often in a burrow/nest, after egg laying; relatively common in amphibians, fish, and invertebrates. Sometimes associated with parental thermoregulation of eggs (e.g., incubation in birds).
Egg brooding	Eggs are carried after oviposition externally or internally in specialized pouches; found in some amphibians, mouthbrooding fishes (e.g., cichlids), insects, spiders, crustaceans, and other invertebrates.
Viviparity	Fertilized eggs are retained within the female reproductive tract during embryonic development; ubiquitous in marsupial and eutherian mammals, more sporadic in squamate reptiles, fish, insects, onychophorans, mollusks, tunicates, echinoderms, arachnids, and bryozoans.
Offspring attendance	Parents remain with offspring after hatching/birth either at a fixed location or by following the offspring as they move around; ubiquitous in mammals, birds, and fish, but also found in insects and spiders.
Offspring brooding	Hatched/born young are carried externally or internally in specialized pouches. External carrying occurs in some frogs, primates, scorpions, and a range of marine invertebrates. Internal carrying occurs in marsupials and mouthbrooding fish.
Offspring food provisioning	Ranges from the transfer of nutrients through a placenta and mass provisioning of brood chambers prior to birth and hatching to progressive provisioning of prey items or specialized secretions (milk) after hatching or birth; ubiquitous in mammals and birds, but also found in some fish, amphibians, insects, spiders, and other invertebrates.
Care after nutritional independence	Offspring are cared for after they have reached the age of nutritional independence, for example, to help offspring in competition with conspecifics or to protect them against natural enemies; found in some birds (cygnets), mammals (hyenas, red squirrels), and insects (burying beetle, earwigs).
Care for mature offspring	Requires long life span and overlapping generations and is correspondingly limited to few taxa. For example, grandparental care in humans: assistance to offspring that have become parents. Other examples include some primates, elephants, and hyenas.

This diversity of form and broad taxonomic distribution of parental care requires an understanding of how and why it evolved. Many organisms do not have parental care. So a key question is, What are the conditions that promote the evolutionary origin of parental care and its maintenance and later modification?

2. ORIGIN AND EVOLUTION OF PARENTAL CARE

By definition parental care enhances offspring fitness. At the same time, it usually comes at a cost to the parents. Parents expend time, energy, and resources delivering care that can impair the parent’s ability to raise other offspring. This evolutionary cost forces parents to balance how much care they direct to an individual offspring against the number of additional offspring they could produce now or in the future. It is only because offspring are genetically related to parents that such behavior may be worthwhile and makes it possible for parental care to evolve. But even when parents and offspring share genes in common, parental care can evolve only if the benefits of care to offspring outweigh the costs to the parent. Why this is so can be illustrated by the following hypothetical example. Imagine a mutation in a female that leads her to stay with her offspring and protect them against predators. Will this mutation increase in frequency in the next generation and spread through the population over time? By being protected from predators the offspring will, on average, have an increased probability of surviving. Half the female’s offspring will carry this mutation, but no other offspring in the population will, and the mutation can spread only if the female directs her care exclusively toward her own offspring. However, even if the female does so, selection does not necessarily favor the spread of the mutation, as it depends on the costs to the female. For example, the female herself may be more exposed to predators by remaining with her offspring, or she may delay or impair her future breeding owing to the time and resources spent on the defense of her current offspring. Thus, answering questions about the origin of parental care requires an understanding of the factors that affect parent-offspring relatedness, the fitness benefits to offspring, and the fitness costs to parents.

Temporary spatial aggregation of parents and their offspring is an important condition that promotes the evolution of parental care for two main reasons. First, it ensures that in an ancestral population where parental care originates, those few individuals that carry a mutation for parental care will pass the benefits of care on to their own offspring, which are also likely to be carriers of the mutation. Second, it increases the probability that parental care can be provided effectively and will improve offspring fitness. If offspring were widely dispersed, it would be more difficult, risky, and time consuming for parents to provide care for their offspring, thus increasing the costs of care to parents. Selection therefore favors the origin of parental care in species that already produce their offspring in clutches or litters and have offspring that remain near the parent for the duration of care.

Variation in life histories of species is another important condition that influences the evolution of parental care. Some organisms develop very quickly, while others have very slow developmental times. Some reproduce only once during their lifetime and produce many offspring in a single clutch or litter (i.e., are semelparous), while others produce their offspring in batches spread over their lifetime (i.e., are iteroparous). If parental care enhances offspring development and thereby the fitness prospects of these offspring, it should evolve more readily in a species with relatively slow development, because the beneficial effect of care can accumulate over a longer period of time. Parental care may also be more likely to evolve when the prospects for future reproduction of parents are low, and the value of the current offspring is correspondingly high.

Irrespective of an organism’s life history, the ecological conditions or hazards faced by parents and their offspring are important determinants of the benefits and costs of parental care. In particular, food availability and natural enemies such as predators or parasites are thought to have played a central role in the origin of parental care. However, it is important to specify precisely how ecological hazards affect parents and offspring. A generally harsh environment will not necessarily favor the evolution of parental care. If harsh environments have negative effects on both adult and juvenile life stages, any potential benefit of care to the offspring may be offset by a high cost to parents. But parental care is much more likely to evolve if the harshness of the environment has a stronger effect on juveniles than on parents. For example, if a main source of mortality is predation by a specialized egg predator that poses no threat to the parent, parental egg attendance might be a very beneficial strategy that should easily spread. Likewise, cannibalism on eggs or offspring by adults from the same species, which is a common phenomenon in many invertebrates, poses typically higher threats on egg and juvenile stages and may favor the origin of egg attendance in a similar way.

There is no single ubiquitous factor that explains the evolutionary origin of parental care across all systems or in a given species. For example, parental protection is not the only possible evolutionary answer to reducing predator-induced offspring mortality. Natural selection can also favor adaptations in the offspring themselves, such as camouflage, that deal with the same hazards. The key factor that promotes the evolution of parental care as opposed to adaptations in offspring is how environmental hazards differentially affect the fitness of parents versus offspring.

3. EVOLUTIONARY MAINTENANCE OF PARENTAL CARE

Once evolved, parental care has a number of important implications for the continuing evolution of a species. In particular, parental care not only is a target of selection but also generates variation in offspring phenotypes and survival. It is therefore also an agent of selection. In this situation, traits expressed in parents and offspring will tend to coevolve with one another owing to selection imposed by the environmental effects of parental and offspring traits on each other’s fitness. For example, the current benefit of food provisioning in many species reflects that juvenile survival of offspring is completely dependent on food provided by parents. It is unlikely that such a dependency would characterize an ancestral population in which food provisioning evolved for the first time, and offspring still retained the ability to forage independently of their parents. Thus, offspring dependency must have evolved secondarily, by coevolving with parental food provisioning and thereby enhancing the adaptive value of provisioning. Conversely, once parental care evolved, conflicts and socially parasitic strategies could have partly undermined the original adaptive value of parental care. As a consequence, studies on the current adaptive value of parental care provide little insight into how parental food provisioning increased offspring fitness in the ancestral state.

The key question then is, What are the main forces that maintain parental care and shape the coevolution of offspring and parental traits? Parents that care for offspring pay a cost by doing so, as they normally cannot remate at the same time. Moreover, the resources parents provide to their offspring cannot also be used to enhance the parents’ own reproduction and survival. These attributes of parental care characterize parental care as an altruistic trait and modify selection during the mating period (sexual selection) as well as selection on life-history traits, such as longevity. Furthermore, following the origin of parental care, the social environment in which offspring develop is partly provided by the parent, which has evolved to enhance offspring development. These forms of social evolution and contingency lead to the coevolution of parent and offspring traits. Finally, because parents and offspring are not genetically identical in sexually reproducing organisms, parental care can induce the scope for genetic conflicts of interest that, in turn, may shape adaptations to family life.

In sexually reproducing species, three social dimensions of within-family conflicts have to be considered: sexual conflict, parent-offspring conflict, and sibling conflict. All offspring have two parents, and the benefits of parental care depend on the combined amount of care provided by the two parents. However, because the costs of care to each parent are determined by the amount of care it provides, each parent would do better if the other paid the costs of care (unless there is lifelong monogamy, without divorce or remating following the partner’s death). This situation leads to sexual conflict over which parent should provide parental care and, in species in which both parents provide care, conflict over the amount of care that should be contributed by each parent.

Sex differences in the provision of parental care are termed sex roles. The most common sex role is female-only parental care, as in most mammals. Male-only parental care also occurs, most notably in some amphibians and some fish; and biparental care, in which both males and females care for offspring, is most common in birds. However, even in species with biparental care the sexes rarely provide parental care in exactly the same way. For example, in many species of birds only females incubate eggs, although both parents may feed nestlings. The two most important factors favoring a divergence in sex roles are sexual selection and certainty of parentage (see chapter VII.3 for a game theory model). The different size of male and female gametes (anisogamy) means that there are fewer female gametes (eggs) than male gametes (sperm). This difference leads to sexual selection in males to locate unfertilized eggs, increasing their benefits of mating effort at the expense of parental effort. Sperm competition as a result of multiple males competing for and mating with females lowers the average relatedness of males to young compared with that of females, further decreasing the benefits of paternal care. This may be especially relevant for males that are successful in mating, who will have mating opportunities elsewhere. However, selection favors male parental care when the population of individuals in the mating pool is very male biased, making the probability of success in mating very low. In these circumstances it is better, on average, for males to invest in offspring that already exist (parental effort) rather than to invest in future offspring (mating effort).

For species in which caring parents interact with their offspring, and especially when such interactions occur over long periods, there is ample scope for offspring to influence the care provided by parents. For example, the mammalian fetus is intimately linked to the mother’s blood circulation through the placenta, and parent birds and some insects make repeated foraging trips to provide food to their offspring. In terms of genetic relatedness, each offspring is of equal importance to parents, but individual offspring are expected to value their own survival and reproduction more highly than that of their siblings. Each offspring is therefore under selection to demand more resources for itself than the parent is under selection to provide, leading to sibling competition and parent-offspring conflict, which are therefore tightly linked. Whenever offspring are produced in clutches or litters, there is opportunity for sibling competition over the limited resources provided by parents. Because parents often initially produce more offspring than they can rear—as insurance against unpredictability of environmental resource availability or hatching failure—demand typically exceeds supply, thus intensifying the conflict. While close genetic relatedness often leads to the evolution of altruism and cooperation, the mismatch between parental supply and offspring demand tends to override any benefits of sibling cooperation. Thus, sibling competition can be extremely severe and involve lethal aggression, as in cattle egrets (Bubulcus ibis), in which older chicks frequently kill their younger siblings.

A large body of theory has shown that parent-offspring conflict is expected to favor the evolution of elaborate forms of communication, such as begging by nestling birds, or high levels of aggression among siblings. Imagine a species in which parental care has recently originated. If parents are sensitive to offspring demands for resources, the genetic conflict favors offspring that exaggerate their demands to manipulate the parents into providing more resources. In a coevolutionary arms race, this form of offspring manipulation generates selection on parents to become less sensitive to these offspring traits, which in turn selects for offspring to increase demand, and so forth, until the conflict reaches an evolutionary stable outcome or resolution. Resolution does not imply that there is no more conflict, just that there are no further opportunities for the manipulation of parents by offspring, and vice versa.

Theoretical models of parent-offspring conflict have shown that evolutionarily stable resolutions of parent-offspring conflict usually require that offspring begging be costly to offspring, thus preventing further evolutionary escalation. Stability is also determined by whether parents or the offspring control the allocation of resources. If parents gain control, and there is selection for offspring to provide costly and honest information about their need or quality, then parents can use that information to allocate resources in a way that optimizes their own fitness. An alternative evolutionary route to resolving conflict is for offspring to gain control over who is being fed by the parent. In that case, the parent has no direct control over the information provided by offspring and allocates resources passively in a way that primarily serves the evolutionary interests of the offspring.

Parental care generates a social environment that is favorable for the growth, development, and survival of offspring. These benefits are intended for the parent’s own genetic offspring but may be exploited by any offspring capable of gaining access to the resources provided by parents, be it from the same or a different species. Parental care generates a social niche for parasitic adaptations that exploit parental behaviors.

Socially parasitic strategies are observed both within and between species. For example, it is well documented that females of some birds such as starlings (Sturnus vulgaris) lay eggs in foreign nests, a behavior called egg dumping. Egg dumping is often used by subordinate females that are unable to breed on their own. By dumping an egg into the nest of a breeding conspecific, they parasitize the caring behavior of the breeder to gain some reproductive success despite not breeding on their own. Social parasitism is not limited to higher vertebrates and can also take place after hatching, as in the European earwig (Forficula auricularia). In this species, nymphs are relatively mobile soon after hatching and can disperse to join other earwig broods, thereby parasitizing the care provided by an unrelated female. While female earwigs tolerate foreign offspring, the nymphs can discriminate unrelated nymphs from siblings and often kill and cannibalize unrelated nest mates. A well-known example of brood parasitism between species is the common cuckoo (Cuculus canorus), which never cares for offspring itself and parasitizes the parental care of a wide range of passerine host species. As obligate brood parasites, cuckoos exhibit a range of highly specialized adaptations to exploit the parental behaviors of their hosts. Female cuckoos lay an egg into the nest of a host species, timed very precisely to avoid detection and rejection by the host parents. The cuckoo chick hatches early and immediately sets about evicting its competitors—the host’s own eggs or chicks. It then uses effective acoustic trickery that makes it sound like a whole brood of host chicks to stimulate its foster parents into providing as much food as they normally provide to a whole brood. The parasitized parents, although typically being much smaller than the cuckoo they feed, provide the rapidly growing brood parasite with all the food it needs to reach independence.

Social parasitism provides a good example of how the original benefits of parental care can be partially undermined once evolved. With increasing frequency of socially parasitic strategies in the population, the evolutionary benefit of parental care is reduced, thereby generating negative frequency-dependent selection on the parasitic strategy and/or selection for defense mechanisms in the hosts (e.g., kin or species recognition). Social parasitism provides a particularly clear example of the important role that social interactions play in driving the coevolutionary processes that result in the evolution and diversification of parental care and associated traits.

4. GENETICS AND EPIGENETICS OF PARENTAL CARE

Parental care must have a heritable basis to evolve, like any other target of selection. But parental care is also an environmental effect that shapes the conditions offspring experience during their development. These transgenerational parental effects can have lasting consequences for trait expression, including the possibility of epigenetic modifications in offspring behavior that are heritable and transmitted to future generations. The complexity of genetic bases of traits expressed in families has a number of interesting consequences for parent-offspring coevolution.

Why do animal families (including humans) typically show considerable variation in the level and duration of parental care and in the intensity with which offspring demand care from the parent and compete with siblings? One explanation is provided by environmental variability. If resources are plentiful, parents can provide all the necessary food for their offspring at relatively low costs. In this case, parental provisioning rate will be high, and as a consequence, offspring resource demand will be low. In contrast, if resources are scarce, provisioning rate will be low—because food is difficult to find—and insufficient for optimal offspring growth, which will lead to high offspring demand.

Recent experimental research shows that variation in parental care may also reflect genetic variation between families in how parents and offspring interact. Why does natural selection not eliminate all the heritable variation and maintain only those parent and offspring genotypes that combine to reflect a unique state of optimally resolved conflict? The main reason is that when parents and offspring interact, parental and offspring traits are determined not only by their own genotype but also by the genotype of the other individual(s) involved. This socially mediated interaction leads to correlational selection favoring particular combinations of parent and offspring traits. Because different combinations are selected, no single parent or offspring genotype will do best in all possible combinations, so genetic variation will be maintained in both parent and offspring traits.

As a consequence of correlational selection, parent and offspring traits become evolutionarily linked, and these traits are therefore also coinherited. For example in great tits (Parus major), burying beetles (Nicrophorus vespilloides), and canaries (Serinus canaria), parents that are good food providers produce offspring that beg more intensely for food. Although this statistical association is robust, the molecular genetic basis for such coinheritance is poorly understood. An exception has been found in studies on laboratory mice based on gene-knockout mutations, which showed that single genes often contribute to some of the variation in the traits of both mothers and pups. One example is the gene Peg3, which affects both milk letdown in females and the suckling efficiency of pups.

From a genetic perspective parental care leads to selection for coadapted (or matching) parent and offspring genotypes that cosegregate within genomes. All parents began their lives as offspring, and all surviving offspring must in turn become parents to gain reproductive success. As a result, genes affecting offspring and parental traits will be located in the same genome, and selection through coadaptation favors physical or statistical association of combinations that are important determinants of how competitive an individual is as offspring and how altruistic it is as parent.

Parental care also plays an important role in the evolution of epigenetic modifications to patterns of gene expression. The best-studied examples involve genes in which only the allele that is inherited from one parent (in some cases the father, and in other cases the mother) is expressed. Such parent-of-origin specific gene expression is termed genomic imprinting. To illustrate how parental care matters in the evolution of genomic imprinting, consider a hypothetical species in which only females provide care, and females care for successive single-offspring litters fathered by different males. The maternally inherited allele should favor a level of care that balances the benefits to the offspring against the costs to the mother’s survival and future reproduction to maximize its transmission to future generations, because the allele will also be transmitted through future half siblings by the same female. In contrast, the paternally inherited allele should favor a level of care that maximizes the benefits to the offspring, because it will not be passed on to future generations through offspring produced by the same female. Theory predicts that genes coding for factors enhancing offspring growth and demand for maternal resources should be expressed when inherited from the father to exploit maternal investment, and silenced when inherited from the mother to limit maternal investment. Evidence consistent with these predictions has been described for a range of genes expressed in the mammalian placenta. An example is the insulin-like growth factor 2 gene (Igf2) expressed in the mammalian placenta, which enhances placental and fetal growth and for which only the paternal gene copy is expressed.

In summary, both the coinheritance of parent and offspring traits favored by coadaptation, and the epigenetic inheritance mechanisms favored by asymmetries in how selection operates on genes inherited from the two parents, reflect how parental care can modify genetic trait architecture, which may feed back to further affect the coevolutionary dynamics of parent and offspring traits.

5. SOCIALITY BEYOND FAMILY

Parental care provides an important stepping-stone toward the evolution of greater social complexity. For example, in some species, the amount of care received by the offspring is determined by the efforts of their parents as well as helpers, that is, other adults in the group that do not themselves breed (see chapters VII.9 and VII.10). The most derived form of sociality is eusociality, which is relatively common among bees, wasps, ants, termites, and—as the only vertebrate systems in which eusociality has been invoked—possibly occurs also in the naked mole rat and the Damaraland mole rat (see chapter VII.13). In these species, the suppression of reproduction of helpers has evolved to such a level that they forgo the opportunity to reproduce entirely.

Close genetic relatedness among individuals is required for the evolution of more complex social groups, including eusociality, and the close association between parents and offspring in many species with parental care is a key stage in this process (see chapter VII.13). More complex forms of sociality can evolve from parental care when selection favors the adult offspring of the parent to stay and help raising siblings (cooperative breeding) rather than dispersing and breeding independently. This evolutionary step requires that care be expressed not only in parents (mated adults pursuing their own reproduction) but also in nonbreeding adults (helpers or workers). This is possible only for forms of care that nonbreeding individuals can actually provide (e.g., progressive provisioning) and if caring is decoupled from mating and reproduction. If the ecological conditions that favor helping persist long enough, helpers may eventually lose the ability to reproduce and become specialized caregivers (often termed workers). Thus, the evolution of parental care represents an important transition that can promote the evolution of ever more complex forms of sociality, such as eusociality.

We have provided a brief overview of the ultimate causes promoting the evolution of parental care (i.e., life history and ecology) and the consequences of that evolution for other phenomena such as evolutionary conflicts, trait inheritance, and sociality. Coevolutionary feedback between life history and parental care traits, mediated by (social) environmental variation and genetic conflicts, makes parental care an evolutionary engine of biodiversity.