Chapter18 Royleetal2012

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The evolution of parental care: summary, conclusions, and implications
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C H A P T E R 18
The evolution of parental care:

summary, conclusions, and
implications
Nick J. Royle, Per T. Smiseth, and Mathias Kölliker
parental interest in the larvae wanes and the rapidly

18.1 Introduction
growing larvae self-feed on the carcass for another
As the light begins to fade in a broad-leafed wood- couple of days before leaving to wander in search
land in England, a male Nicrophorus vespilloides of a suitable place to pupate.
burying beetle, guided by olfactory cues picked up If you are familiar with Nicrophorus burying bee-
by his feathery antennae, alights on the carcass of a tles, whose common name in England is the sexton
gently decomposing wood mouse. After a thorough beetle after their ‘grave-digging’ exploits, then the
inspection of the carcass, he stands on top of the natural history account sketched above will come
mouse, lowers his head, raises his abdomen, and as no surprise. To most other people however this
squirts a cocktail of pheromones into the air. The level of complex parental care in an insect might
response to his calls is rapid. A female N. vespilloides raise an eyebrow at the very least. Why do bury-
arrives within minutes. He mates with her almost as ing beetles provide parental care at all? How did
soon as she lands. But the calls have also attracted it evolve from a non-caring ancestor? Why do par-
another male. As the female begins the process of ents go to all the trouble of defending the carcass
burying the mouse the male defends the prized against all comers, and actively provision the pre-
carcass from his rival. They are evenly matched in pared food to begging offspring? Why not just lay
size but the fight is brief, with the resource-holding some eggs and then leave them to hatch, grow,
male victorious and his defeated rival sent scuttling and develop on their own like the blow flies that
through the leaf litter to look for opportunities else- also buzz around the carcass? Parental care is often
where. The victorious male and the female jointly costly to the parents, so how and why does it persist
bury the carcass, pausing only to mate, lay eggs once it has evolved? Why do parents stick around
in the soil nearby, and defend the carcass against after laying eggs next to a substantial source food
other species of marauding beetles and slugs, before for their offspring rather than use it to enhance
they strip the mouse of fur. By the time the eggs their own survival and the production of a larger
hatch, some 60 hours after laying, the larvae wriggle number of offspring? What determines whether it
their way to the carcass where the parents have is males or females or both parents that stay to pro-
created a bowl-shaped crater in the body of the vide care? Why do males and females often have
mouse containing a soup of partially digested meat. different roles? How much care should be provided,
In addition to feeding directly on this soup, the how much should each parent contribute, and how
tiny larvae also rear up and touch the parents with should available resources be allocated among indi-
their legs, begging to be fed. The female obliges by vidual offspring?
regurgitating food for them. Meanwhile the male These sorts of questions are applicable to any
industriously patrols the carcass, keeping it free species with parental care and are by no means
of microbes and mould. Three days after hatching limited to burying beetles. Parental care is taxonom-
The Evolution of Parental Care. First Edition. Edited by Nick J. Royle, Per T. Smiseth, and Mathias Kölliker.
© Oxford University Press 2012. Published 2012 by Oxford University Press.
328 T H E E VO L U T I O N O F PA R E N TA L C A R E
ically widespread (see Chapters 1, 4, and 5) and is beyond the minimum level needed for successful
central to the maintenance of biodiversity through fertilization, and that the increase in provisioning
its close association with other phenomena, such evolved or is currently maintained to enhance off-
as sexual selection, life-history evolution, sex allo- spring fitness.
cation, sociality, cooperation and conflict, growth There is an important difference between
and development, genetic architecture, and pheno- a conceptual definition of parental care and
typic plasticity. This book provides an overview of operational modifications to it. Conceptually, the
the current state of the study of the evolution of definition has to be broad and should be based
parental care, and the previous 17 chapters pro- on the ultimate functional context. Operationally,
vide in-depth analyses of the major themes. In this a definition of parental care can include useful
chapter, we provide a summary of the key points proximate criteria that are specifically suited to the
addressed in the previous chapters, draw some con- question being addressed. The latter approach may
clusions, and consider future directions in the field. be more appropriate when discussing the origins of
particular forms of care from a state of no care and
when considering patterns of care across species or
18.2 What is parental care?
between the sexes (Chapter 2). Chapter 1 discusses
Parental care is a purely descriptive term, which in detail definitions of other key terms used in
does not take account of any costs to parents of the study of parental care, and advocates a more
providing care, and can be broadly defined as ‘any consistent usage of these terms and definitions in
parental trait that increases the fitness of a parent’s future studies of parental care.
offspring, and is likely to have originated and/or
is currently maintained for this function’ (Chapter
1). This definition includes non-behavioural traits, 18.3 Origin and evolution
such as gamete provisioning, gestation, vivipar- of parental care
ity, and nests, but excludes mating behaviours
18.3.1 Costs and benefits
that increase offspring fitness, such as the defence
of breeding territories, unless there is evidence At the simplest level, parental care is expected
that such behaviours evolved and/or are currently to evolve when the benefits of providing care
maintained because they enhance offspring fitness outweigh the costs (Chapters 2 and 3). Providing
(Chapter 1). The latter condition is the key to the care is beneficial to offspring as it neutralizes
definition. For instance, many researchers exclude environmental hazards, but is costly to parents as
gamete provisioning as a form of parental care it utilizes resources that parents otherwise could
because all animals show some form of gamete have allocated to their own survival or future
provisioning. If gamete provisioning were classified reproduction (Chapters 1 and 3). The benefits and
as parental care, then all species with anisogamy costs are split across the generations, so parental
would potentially be classified as species with care will be under antagonistic selection in parental
female care. So, should all species with anisogamy and offspring life-stages (Chapters 1 and 16). There
be considered as showing a form of female care for is selection for receiving care when individuals
offspring? The answer is no. Anisogamy and provi- are offspring because care increases fitness, but
sioning of resources to gametes by females evolved there is selection against providing care when
due to gamete competition leading to disruptive individuals are parents because the costs of care
selection favouring the production of small and reduces fitness (Chapter 1). However, selection
competitive gametes (sperm) by some individuals on offspring can generate a correlated response
(males) and the production of large and nutrient- in parents due to the close relatedness of parents
rich gametes (eggs) by other individuals (females) and offspring (Chapters 15 and 16), which allows
(Parker et al. 1972). Gamete provisioning should parental care to evolve (Chapter 1). Understanding
only be included as a form of parental care if it can the evolution of parental care therefore requires
be demonstrated that the level of provisioning is separating out parental and offspring fitness to
T H E E VO L U T I O N O F PA R E N TA L C A R E : S U M M A RY, C O N C L U S I O N S, A N D I M P L I C AT I O N S 329
avoid double counting (e.g. erroneously assigning models show that selection favours parental care
offspring survival to both parental and offspring when egg or juvenile mortality in the absence of
fitness; Chapter 1). care is high, and the duration of the egg or juve-
Parental care can increase offspring fitness by nile stage is relatively long (Chapter 2). However,
affecting offspring survival directly or indirectly there has been surprisingly little empirical research
via effects on offspring phenotypes that, in turn, on the relationship between ecology and the prob-
affect offspring survival (Chapter 14). Conversely, ability of the evolution of parental care, so this is
parental care can reduce parental survival and therefore an important topic for future research.
future mating and reproductive success (Chapter The evolutionary origin of parental care may also
2). Benefits to offspring may be short term, as in be enhanced by the presence of behavioural pre-
bromeliad crab where parental manipulation of cursors or incidental parental effects that can be
pH in breeding pools through the addition of snail modified into parental care. For example, guard-
shells and removal of organic matter improves ing of eggs and offspring is likely to have evolved
the conditions for offspring development. from ancestral defensive or aggressive behaviours
Alternatively, parental care may have delayed in non-caring species (Chapter 1), especially when
benefits to offspring, as in some species of bird parents recognize and/or regularly encounter their
where increased provision of carotenoids in eggs own genetic offspring (and the benefits of care
affects the expression of sexual ornaments in are not outweighed by the costs associated with
adulthood (Chapter 3). Other benefits such as increased competition with close kin, as may occur
direct provisioning of post-natal offspring by in viscous populations; Chapter 2). In some taxa,
parents may have immediate (reduced probability attendance of eggs is associated with an increase
of starvation), medium (increased growth and in egg size (Chapter 2), suggesting that large eggs
development), or long-term effects (e.g. increase in may favour egg attendance and/or that egg atten-
cognitive ability in adult blue tits Cyanistes caerulens dance may favour large eggs. Once care has orig-
due to a spider-rich diet, high in taurine, when a inated such co-evolutionary feedback loops may
nestling; Arnold et al. 2007). lead to the rapid evolution and diversification of
other parental care traits, especially given that nat-
ural selection is expected to favour a tight phe-
18.3.2 Evolutionary origins
notypic integration of parental traits and offspring
Early attempts to understand the origin of parental development (e.g. altriciality) (Chapter 14). Thus,
care emphasized the role of environmental pres- evolutionary loss of care may be rare once complex
sures, such as the harshness of the environment and care has evolved (Gardner and Smiseth 2011) as the
the use of rich, but ephemeral, resources (Chapters social environment provided by family members
1 and 5). Whilst ecological conditions appear to becomes an important determinant of development
be an important factor driving the evolution and and reproduction and, hence, the persistence and
diversification of care in some taxonomic groups maintenance of parental care.
(e.g. breeding pool size is associated with the evo-
lution of parental care in frogs; Brown et al. 2010),
18.3.3 The role of the social environment
the stability, structure, and harshness of the envi-
ronment alone does not usually explain the evo- The social environment is important to the
lutionary origins of care (Chapter 1). For example, evolution of parental care because behavioural
extended parental care is relatively rare in insects, interactions and the transfer of resources and
even though exposure to harsh environments is information between parents and offspring shape
common (Chapter 5). Nevertheless, environmental the development of phenotypes. Parents trans-
variation may indirectly affect the likelihood that fer a diversity of non-genomic resources to off-
parental care evolved by altering patterns of mor- spring that are essential for development (e.g.
tality in parents or offspring, or developmental time maternally-derived mDNA and RNA and various
in offspring (Chapter 2). For example, theoretical proteins and hormones; Chapter 14). In fact, it is
the transcriptional machinery that females add to vide a form of insurance against the failure of core
eggs that allows the inherited DNA to be tran- chicks (replacement offspring; Mock and Parker
scribed and have effects on offspring phenotype. 1997). However, overproduction also means off-
Such parental effects often continue throughout offspring demands often exceed parental supply, cre-
spring development, may have long-term effects, ating the social environmental conditions for con-
and take a variety of forms ranging from the pre- flicts of interest over parental investment among
natal maternal transfer of transcriptional factors family members (Mock and Parker 1997; Chapter 8).
and macro-and micronutrients, through to provi-
sioning of resources to young after hatching or birth
and the behavioural transmission of information 18.4 Conflicts and cooperation in
through learning or imprinting mechanisms. The parental care
origin of variation in parental effects begins with
18.4.1 Why are conflicts expected?
a responsive phenotype (phenotypic accommoda-
tion; Chapter 14). Such responsiveness to changes Evolutionary conflicts arise because parental care
in the environment often has a genetic basis that is an altruistic trait that incurs costs to the par-
varies among individuals, and is therefore herita- ents (Chapter 3) and because the providers of care
ble. Consequently, there is considerable scope for (parents) and recipients (offspring) are not perfectly
the genetic variation underlying phenotypic accom- related to one another in sexual organisms (i.e.
modation to be shaped by selection (genetic accom- do not share all genes in common). This means
modation; Chapter 14). Phenotypic accommodation that a behaviour that maximizes the fitness of one
by parents therefore allows parental effects to be individual does not necessarily maximize the fit-
carried over across generations (e.g. pre-natal expo- ness of others (Chapters 7, 8, and 9). Sexual con-
sure to maternal hormones can epigenetically reg- flict among parents over parental investment is an
ulate gene expression in offspring; Chapters 14, almost inevitable consequence of sexual reproduc-
17, and Section 18.6.2), providing a link between tion because the two parents are typically unre-
the environment experienced by parents and that lated to one another, even if they do have shared
experienced by their offspring. Parental effects may interests in their common offspring and may coop-
therefore provide an important source of informa- erate to raise young together (i.e. biparental care;
tion for offspring if the environmental conditions Chapter 9). Parent–offspring conflict (POC; Chap-
experienced by parents and offspring are correlated ter 7) and sibling competition (Chapter 8) over
(Chapter 14). parental care occur even though the individuals
Parents often respond to environmental unpre- involved are close relatives. In these cases asym-
dictability by producing more offspring than can metries in relatedness between parents and off-
normally be reared. Such overproduction may rep- spring and among siblings generates different opti-
resent a bet-hedging strategy, allowing parents to mal levels of care for parents and each individual
simultaneously track variable resources in the envi- offspring.
ronment and increase their control over resource The extent of conflict is determined by the differ-
allocation within the brood. Mothers can poten- ence among optima for family members (the ‘battle-
tially manipulate the social environment that off- ground’), or by the amount that each member’s fit-
spring experience through hatching asynchrony, ness is below its optima (the ‘conflict load’) (Chap-
which in birds is largely the consequence of early ter 9). As a result, there is evolutionary conflict
onset of incubation, creating a structured family even in situations where individuals are not directly
where first-hatched ‘core’ chicks enjoy substan- interacting with one another and where there is
tial fitness advantages over last-hatched ‘marginal’ no overt conflict or aggression among interacting
chicks (Mock and Parker 1997; Forbes 2009). The individuals (Chapter 7). This is because the con-
creation of a structured family through phenotypic flict refers to the way in which selection acts on
handicapping of some offspring can ensure that family members, not the expression of behaviours
parents can more easily match the brood size to the such as fighting (Chapters 7 and 9). The outcome
current conditions (resource tracking) and/or pro- of these conflicts of interest (the ‘resolution’) is the
critical determinant of how parental resources are plex relationships between OSR, sexual selection,
transferred from parents to offspring (Parker et al. certainty of parentage, and the adult sex ratio (see
2002), and affects the evolutionary stable mode of Fig. 18.1 and Chapter 6).
care expressed (i.e. uniparental or biparental care;
Chapter 9).
18.4.3 Sexual conflict over care
Models of offspring desertion predict that
18.4.2 Who should provide care?
biparental care will be favoured when two parents
Which sex provides care depends on a variety of are more than twice as good at raising offspring
factors including the mode of fertilization, how as a single parent (Chapter 9). Desertion of
selection acts on males and females and the cer- offspring is more likely when a single parent is
tainty of parentage. In external fertilizing species, nearly as effective as a pair, with the deserting
trade-offs between growth and reproduction are parent most likely to be the one that is least
important determinants of sex roles in parental effective at parenting and expressing the most
care. In fish, for example, male-only care is more strongly sexually-selected traits (typically, but not
likely in species with external fertilization, which always, males; Chapters 6 and 9). However, the
may be because larger females usually have higher probability of desertion also depends on available
fecundity and indeterminate growth, but reproduc- opportunities elsewhere. If the OSR becomes
tion diverts resources away from growth, favouring more male biased and sexual selection intensifies,
male-biased parental care (Gross 2005). In species uniparental female care becomes more likely as
with internal fertilization, whichever sex provides the initial difference between the sexes in parental
parental tissue is best placed to carry on provid- care becomes self-reinforcing and the number
ing care, which is most often, but not always (e.g. of successful males gets smaller and smaller
seahorses; Paczolt and Jones 2010), females (Chap- (Lehtonen and Kokko 2012; Fig. 18.1). However,
ter 6). However, the primary determinants of sex biparental care is favoured if sexual selection
roles during parental care are sexual selection and is relaxed at a high OSR, and the proportion of
the certainty of parentage (Chapters 2, 6, and 11). successful individuals of the more common sex
In internally fertilizing species, maternity is typ- increases (Chapter 6), due to reduced ability to
ically more certain than paternity because females monopolize matings, for example (Chapter 2).
often store sperm from previous mating with other Biparental care is a form of cooperation between
males, which has the effect of reducing the relat- parents to rear young together. However, when the
edness between a male and the offspring that he costs of providing care are not aligned with the
might care for (Chapter 11). Thus, sperm compe- parents’ future reproductive interests (i.e. no ‘true’
tition reduces the certainty of parentage, which monogamy; Parker et al. 2002), there may be con-
in turn reduces the benefits of providing post- flicts of interest over how much each parent should
zygotic care to males (Chapters 2, 6, and 11). Sex- contribute to this joint investment. The majority of
ual selection in males to locate unfertilized eggs models of sexual conflict over care predict that the
increases the benefits of mating effort at the expense focal parent should respond by partial compensa-
of parental effort for males. However, selection tion to a change in investment by its partner; a
favours male parental care when the proportion prediction that is broadly supported by experimen-
of individuals available to mate in the population tal empirical data across a wide range of species
(the operational sex ratio; OSR) is very male biased, (Harrison et al. 2009). New models that incorpo-
making the probability of success in mating very rate costs of negotiation between parents show that
low (Chapter 6). In these circumstances it is bet- when both parents care together for offspring, the
ter on average for males to invest in offspring that ESS levels of relative investment are low early on in
already exist (parental effort) rather than investing breeding. However, the levels increase throughout
in future offspring (mating effort). As a result sex the period of parental care because opening bids
roles in parental care are determined by the com- of investment by one parent provides information
Increased benefits of
male care
Low Cost of
care
Conflict
Cost of
Probability of mating High
care Adult
success
Reduced benefits of Sex Ratio
male care
Reduces sexual selection
to locate unfertilized
Reduced confidence
eggs
of percentage
Sperm Increased mating

competition effort
Sexual selection to
locate unfertilized Multiple
eggs mating
Male-biased Positive or Female-biased

OSR negative effect OSR
Figure 18.1 Who provides parental care? Anisogamy means that lots of small gametes (male) compete for access to small numbers of large gametes
(female), which leads to a male-biased OSR. Sperm from several males seeking out the same egg before fertilization (multiple mating) results in sperm
competition, which makes it harder for a male to identify his own young (lowering confidence of parentage), reducing the benefits of male care and
increasing the benefits of investing resources in locating unfertilized eggs (mating effort), making the OSR even more male-biased. This leads to stronger
sexual selection on males to locate unfertilized eggs, so that a male in a population with a male-biased OSR can prioritize investment either in his offspring
that already exist (parental effort) or offspring that may never exist (mating effort). If the OSR becomes male biased this will reduce the probability of
success in mating for the average male, which will select for increased male parental effort, but for a subset of males success in mating may increase,
selecting for reduced parental effort and greater mating effort. This subset of males is important as selection acts on the parenting decisions of all males
that mate. Whether uniparental care or biparental care evolves depends on the strength of the sexual selection on males, and other factors such as the
independent effects of the adult sex ratio (ASR) on the OSR. If costs of parental care influence the ASR, through, for example, increased mortality of the
caring sex, then this will feedback to the OSR, leading to relaxed sexual selection to locate unfertilized eggs and increased selection for male care
(if the caring sex is female) because the caring sex is rarer in the population. Conversely, if the non-caring sex (males) experiences higher mortality then the
caring sex becomes more common, strengthening sexual selection on males.
that can be exploited by the other parent, but later effects of conflicts between other family members
on in reproduction this is not possible (Lessells (Chapter 9).
and McNamara 2012). As a result of such sexual
conflict, parents are expected to withhold parental
18.4.4 Sibling competition, cooperation,
investment, thereby lowering the offspring’s fitness
and parental favouritism
(e.g. Royle et al. 2002a). Alternatively parents may
monitor each other continuously throughout the The combination of initial overproduction of off-
period of parental care, such that the ESS is for spring by parents, relatedness asymmetries, and
parents to alternate who provides care; in which limited resources means that sibling relationships
case the behavioural coordination between parents are often agonistic. Interactions among siblings can
acts as a form of reciprocity that reduces sexual involve sublethal competition (e.g. non-aggressive
conflict (Johnstone et al. submitted; Chapter 9). The scramble competition for parental resources as in
exact evolutionary outcome of sexual conflict over altricial birds competing for access to food pro-
care depends not just upon the behavioural mech- vided by parents) and lethal competition (e.g. direct
anisms used by parents to negotiate care, but also violent attack leading to death as in many birds
the shape of the offspring benefit curves and the of prey). However, in some species, siblings may
cooperate to secure more resources from parents resources (Chapters 7 and 16). Parents may not
(e.g. coordinated begging; Black-headed gulls Larus have full control of resource provisioning because
ridibundus, Mathevon and Charrier 2004; Banded offspring have ‘private’ information about them-
mongooses Mungo mungo, Bell 2007), or reduce the selves (e.g. their condition or state) that would be
costs of competition through negotiation (e.g. Barn beneficial to the parents to know in order to max-
owls Tyto alba, Chapter 8). Parental allocation of imize parental fitness (Chapter 7). Offspring can
resources to offspring is rarely equal (Mock and exploit the parents’ lack of information by exag-
Parker 1997). Parental favouritism can occur when- gerating their true needs in order to gain more
ever there are fitness benefits to parents of differ- parental investment than would be optimal for par-
ential investment among offspring (e.g. differential ents to supply (Chapter 7). As a result, the amount
allocation of resources to male and female offspring, of parental resources provided to offspring at con-
also termed sex allocation; Chapter 10). Parental flict resolution depends critically on who controls
favouritism can increase competition among sib- resource allocation—parents or offspring (Royle
lings for access to parental resources, leading to et al. 2002b). Parental control is more likely in gen-
conflicts of interest between parents and offspring. eral when the rate of provisioning is genetically or
physiologically constrained or when resource avail-
ability is highly predictable (Chapter 7). However,
18.4.5 Parent–offspring conflict
in reality control is likely to be on a continuum,
Conflict between parents and offspring can occur ranging from full parental to full offspring control,
over both the total amount of parental investment and changing dynamically during ontogeny and in
supplied (interbrood conflict) or the distribution of response to variation in the (social) environment
parental investment among offspring (intrabrood (Royle et al. 2002b). Co-adaptation models explore
conflict). Interbrood conflict leads to selection for how genetic variance and covariance of interact-
offspring to extract more resources from parents ing traits expressed in parents and offspring are
at the expense of future siblings (Chapter 7). In expected to co-evolve, with correlational selection
contrast, intrabrood conflict leads to selection for essential for this to occur (Chapter 16).
mechanisms by which offspring bias the distribu-
tion of parental resources at the expense of current
18.5 Co-evolution and correlated
siblings (Chapters 7 and 8). Optimal strategies
responses
can differ at different stages of life for the same
individual (i.e. when a parent compared to when an Correlational selection occurs when selection
offspring; Chapters 7 and 16). In order to provide favours particular combinations of traits.
empirical evidence for POC the battleground of Co-adaptation models show that correlational
conflict must be established (i.e. show that optimal selection via social epistasis can be strong enough
levels of parental investment differ between to select for parent–offspring covariance even
parents and offspring) and any change to the way if loci are unlinked (Chapter 16). In such cases,
in which parental investment is allocated should offspring traits are affected by an interaction
then lead to an increase in fitness in one party at between direct effects of genes expressed in
the expense of the other (Chapter 7). For example, offspring and indirect effects of genes expressed in
experimental manipulation of gene activation parents, with selection operating on the outcome
in mice shows that paternally expressed alleles of the interaction between parents and offspring.
lead to larger offspring via increased demand for However, selection is required to maintain parent–
maternal resources, because paternally derived offspring covariance, otherwise recombination can
alleles are evolutionarily not limited by any costs of lead it to break down within a few generations.
maternal care (Haig and Westoby 1989; Chapters 7 Hence, factors that limit recombination between
and 17). correlated parent–offspring traits, such as
At the heart of parent–offspring relations is the pleiotropy (e.g. the Peg3 gene that affects maternal
co-evolution of demand for, and supply of, parental milk let-down and offspring suckling behaviour in
mice; Curley et al. 2004) or linkage disequilibrium of variation underlying these relationships (Chap-
(e.g. via assortative mating), should be favoured ters 15 and 16). Such co-evolutionary effects are not
by selection (Chapter 16). Empirical evidence for confined to parent–offspring interactions. Despite
parent–offspring co-adaptation comes mainly from widespread recognition that behaviour during mat-
cross-fostering or line-crossing studies, which ing strongly influences patterns of parental care
test whether the genetic origins of parents and (Chapters 6 and 11), empirical support for pre-
offspring, and the social (family) environment dicted relationships between mating behaviour and
in which they are expressed, are matched or patterns of parental investment remains equivo-
mis-matched (Chapter 16). Furthermore, there is cal (Alonzo 2010). For example, males are pre-
also evidence from molecular studies showing dicted to decrease their parental effort in response
an increasing number of genes that influence to a decrease in paternity if there are oppor-
both maternal care and offspring behaviour in tunities for higher paternity in the future, and
laboratory rodents (Chapter 17). These empirical females are expected to choose males based on
studies show considerable variation in the sign male traits that indicate his genetic quality (Chap-
of the genetic correlation between parental and ters 6 and 11). Neither of these predictions have
offspring behaviours, including, in some cases, widespread empirical support (Alonzo 2010; Chap-
no correlation between the two despite heritable ter 11). This may be because research has focused
variation in both parental and offspring behaviours on pairs of traits and ignored social dynamics
(Chapters 7 and 16). This pattern most likely and co-evolutionary feedbacks among interacting
reflects the dynamic nature of parent–offspring individuals (Kölliker et al. 2005; Alonzo 2010).
co-adaptation and differences between systems in Traits that protect paternity in particular might
the extent that parents versus offspring control the be expected to co-evolve with care (e.g. repeated
interaction (Chapters 7 and 16). mating rate or nuptial gifts; Chapter 6). Such co-
Most co-adaptation models do not allow par- evolution can be examined by applying artificial
ent and offspring response rules to evolve (Chap- selection to the traits of interest. For example,
ter 16), and therefore provide only limited insights selecting for rate of mating is expected to lead to
into the stability of parent–offspring interactions. changes in the expression of social traits in males
Understanding the dynamics and stability of co- in the context of parental care, which then feeds
adaptation requires the use of a behavioural reac- back to change the expression of behaviour of
tion norm (BRN) approach, which focuses on the females in the context of mating, and so on. This
co-evolution of behavioural response rules (Smiseth social feedback loop is expected to have conse-
et al. 2008). Recent models suggest that selection quences for the relationship between parents and
should act on BRNs to stabilize parent–offspring offspring, with changes in parental care behaviours
interactions in such a way that parent–offspring co- expected to lead to changes in offspring behaviour,
evolution is associated with variance in behaviours which modify parental behaviour, and so on, form-
over time, not just mean levels of behaviour (Dobler ing a feedback loop of co-evolution across traits
and Kölliker 2009). These forms of co-evolutionary expressed in different functional contexts (Alonzo
dynamics are complex because parents exert selec- 2010).
tion on offspring phenotypes, and, if offspring Feedback loops are likely to be important in the
influence parental care, offspring also exert selec- co-evolution of brood parasites and their hosts.
tion on parental phenotypes (Chapter 15). Further Parental care generates a social environment that is
development of indirect genetic effect models is highly favourable to the growth, development, and
necessary to clarify exactly how selection acts on survival of offspring, thereby generating a niche
parents and offspring to determine co-evolution in that social parasites can exploit. Because parasitic
families (Chapter 15). young are unrelated to their foster siblings, and
Models of co-adaptation illustrate how parental have no shared interests in the fitness of their
care evolves as a consequence of the outcome of hosts, brood parasitism provides a suitable model
family interactions and the heritable components to examine the limits of selfishness in parental
care (Chapter 13). The dynamics of co-evolution mimicry to procure food, may be more costly
between parasites and hosts depends on the viru- to the host parents’ future success because they
lence of the parasites, as this determines the social use host chicks to secure more parental invest-
environment that the interactions take place in and, ment (Chapter 13). Consequently the relationship
by definition, the costs of parasitism to hosts (Chap- between virulence and the costs of parasitism may
ter 13), thus leading to negative density-dependent be complex.
selection on the parasitic strategy (the higher the Why do host parents have such difficulty in
density, the lower the fitness for the parasite due to detecting parasitic offspring? One reason may be
reduced availability of hosts). Host defences may be that the system is still dynamically co-evolving, and
constrained by high costs of defence relative to costs there is an evolutionary lag in the host’s defence.
of parasitism (Chapter 13). During the offspring- Alternatively, the parasite and host may be in evo-
rearing stage more apparently highly virulent par- lutionary equilibrium, but the costs of defence may
asitic offspring may actually impose lower costs to be greater than the costs of accepting brood para-
the host’s residual reproductive success than appar- sites (Chapter 13). As host susceptibility tends to
ently more benign parasites. For example, common be the rule, and there are few examples of counter
cuckoos use vocal and visual signals to procure defences by host parents at the chick-rearing stage
food from host parents, but the relatively small gape of development (Chapter 13), it is likely that the
area they present compared to a whole brood of latter is true in most systems. Such co-evolutionary
host nestlings limits the rate at which they are fed relationships are likely to be common features not
by their foster parents (Chapter 13). Less obviously just of host–parasite dynamics, but also of the net-
virulent parasites, such as brown-headed cowbirds, work of relationships and interactions among fam-
that are raised alongside host chicks and that use ily members (Box 18.1).
Box 18.1 Social networks in the context of parental care
How individuals interact with one another can have 2003). This is more realistic as it views the behaviour of
important consequences for the expression and evolution of individuals as being both the cause and the effect of their
phenotypic traits (e.g. Chapters 7, 8, 9, 15, and 16). The social environment (Wolf and Moore 2010; Chapter 15).
outcomes of such behavioural interactions can affect A social networks approach has been instrumental in
patterns of organization and structure at a variety of advancing our understanding of numerous areas of
different levels, including colony-level effects (Linksvayer behavioural and evolutionary ecology including the
et al. 2009), population-level effects (Plaistow and Benton evolution of animal societies, cooperation, and the
2009), and even ecosystem-level effects (Gribben et al. transmission of disease (reviewed in Sih et al. 2009), but
2009). The genetics and evolutionary dynamics of social has rarely been applied to the study of parental care. In fact
effects depend critically on the structure of social there are very few studies that have even examined the
interactions (Wolf and Moore 2010; Chapters 15 and 16). relationship between measures of fitness and social
However little is known empirically about the structure of network parameters. Two studies have quantified how
social interactions; the processes involved are a ‘black box’. social position within a network is related to the fitness
The emerging field of social networks analysis provides a prospects of interacting individuals in the context of mate
potential tool to unlock this box. choice/sexual selection (McDonald 2007; Oh and Badyaev
The social environment an animal encounters typically 2010), but we are not aware of any research on the
consists of a complex network of non-random and highly relationship between fitness outcomes and the structure of
variable social interactions (Croft et al. 2008; Fig. 18.2). the network of interactions themselves in any social
Studies of social behaviour that incorporate a network context. This seems surprising because this information is
approach shift the focus from variation in behaviour among central to understanding the evolutionary and ecological
individuals per se to how interactions among individuals significance of social interaction networks (Fewell 2003; Sih
shapes variation in behaviours and phenotypes (Fewell et al. 2009).
Box 18.1 (Continued)
Understanding the resolution of conflict during interactions as a network (Godfray and Johnstone 2000; Parker et al.
among family members in species with parental care is one 2002; Kölliker 2005). The reason that family interactions
area that would particularly benefit from integrating tend to be modelled as multiple dyadic relationships is not
information on fitness and network structure. only due to mathematical tractability, but also a lack of
Communication among individuals in animal families empirical data. For example, altricial bird nestlings often
involves a network of (often simultaneous) interactions, interact with each other and feeding parents through
among siblings, between parents and offspring, and begging competitions and by jostling for positions close to
between male and female parents (Horn and Leonard the feeding parent (Horn and Leonard 2005; Kölliker et al.
2005). The resolution of conflicts of interest over the 1998; Hinde et al. 2010). These begging displays and the
provision of parental investment in families (Chapters 7, 8, dynamics of their movements in relation to other family
and 9) implicitly involves a network of multiple interactions, members within the nest therefore shape brood social
not just multiple dyadic interactions among individual structure (Fig. 18.3), but empirical studies do not explicitly
members (Parker et al. 2002), but is not usually modelled account for this (Horn and Leonard 2005).
Figure 18.2 A toy social network showing interactions (lines—or ‘edges’) among individuals (circles—or ‘nodes’). One individual (the black node)
provides a key link in the network, between the two subgroups, even though it is not directly connected to all individuals in the network. The
importance of this link would not be obvious using traditional, but widely-used, techniques that only consider pair-wise (dyadic) interactions between
individuals. Such links in the network are likely to be particularly important for the transfer of information and pathogens.
(a) (b)
Figure 18.3 Representative networks of begging great tit nestlings associating with one another during feeding by parents: (a) Social network for
a strongly-connected brood of eight nestlings, and (b) Social network for a weakly-connected brood of eight nestlings. Experimentally food-deprived
nestlings are shown in white, experimentally satiated nestlings in black, and un-manipulated nestlings in grey. The thickness of the lines (edges)
indicates the strength of the connection between individuals (nodes). Associations among nestlings are non-random and connectedness within broods
is related to hunger (food-deprived nestlings have a greater strength of associations than satiated nestlings) in both networks, even though the
networks differ in overall connectedness.
There are several other features of social interactions likely to interact with multiple individuals in the network on
within families of species that are reared in nursery multiple occasions and group membership is clearly
environments that make them ideal study systems to defined, it is possible to make use of weighted (as opposed
quantify between-group consequences of variation in social to binary) network metrics. Consequently the quality of
network (family) structure on fitness. In contrast to many information available in constructing the social networks is
social networks analyses, where it can be difficult to assign high, and allows measures of the strength of behavioural
individuals to groups, there are no ‘gambit of the group’ interactions to be incorporated (Whitehead 2008). Finally,
issues (Croft et al. 2008). This is because all offspring within the use of interacting family members makes it possible to
each nursery can be clearly and unambiguously assigned to quantify the fitness consequences of variation in social
a given group, and there is unlikely to be movement of interactions among individuals at levels of selection higher
offspring between nurseries, so each brood represents a than the individual through the use of replicated networks,
discrete network of individuals (or subnetwork if parents which is an important step on the path to establishing how
interact with other parents during, for example, foraging for the structure of social interactions co-evolves with traits
food). In addition, because each individual within a brood is involved in parental care (e.g. Fehl et al. 2011).
18.6 Mechanisms and constraints to some extent by introducing state variables

in parental care that characterize current physiological state (e.g.
hunger, condition etc; Chapter 3), it illustrates the
The proximate mechanisms underlying variation in potential issues involved in making simplifying
the costs and benefits of care are important deter- assumptions about resource allocation decisions.
minants of (co-)evolutionary trajectories that can be Similarly, resource acquisition may involve intrin-
broadly classified as being genetic or physiologi- sic trade-offs between specific components of diet
cal in origin. Whilst these often provide constraints that would not be accounted for if the currency of
on evolution the mechanisms themselves can also acquisition was assumed to be just energy (Chap-
evolve in response to selection to shape phenotypes. ter 3). For example, different ratios of protein to
carbohydrates in the diet are optimal for increas-
ing egg production compared to increasing lifespan
18.6.1 Physiological mechanisms
in Drosophila (Lee et al. 2008). Oxidative stress is
Cost–benefit approaches to the study of parental a potential mechanism underlying these costs that
care, where resources are often considered to be has recently been suggested to be a key proximate
limited (i.e. only available to spend once) and the constraint on the evolution of life-histories, includ-
common currency is usually assumed to be energy ing parental care (e.g. Metcalfe and Alonso-Alvarez
or time, have been central to the development of 2010).
theory and underlie most empirical studies (Chap- Oxidative stress occurs when there is an imbal-
ter 3). However, until relatively recently there has ance between the production of reactive oxy-
been little work on the physiological mechanisms gen species, which are byproducts of normal
that govern these trade-offs. One of the main prob- metabolic processes, and the availability of antiox-
lems with the traditional approach is that parents idant defences in favour of the former (Metcalfe
and offspring may not both be drawing from a and Alonso-Alvarez 2010). There is substantial evi-
common pool of resources (known as the ‘com- dence for oxidative stress as a cost of parental care
mon currency problem’; Houston and McNamara from a growing number of experimental studies,
1999). The resources required by offspring may dif- mostly on birds (Chapter 3). However, there are
fer from those required for somatic maintenance relatively few studies that demonstrate long-term
by parents (e.g. parent Palestine sunbirds Nec- effects of oxidative stress on correlates of fitness
tarinia osea feed on flower nectar, but their off- (e.g. Alonso-Alvarez et al. 2006), and most of these
spring are fed arthropods; Markman et al. 2002). are observational rather than experimental stud-
Although this problem can be addressed in models ies (Chapter 3). An increase in parental effort can
also lead to suppression of the immune system, variance in parental behaviour; Chapter 17), but
although this effect is often an indirect consequence that multiple genes influence parental behaviour.
of other physiological costs such oxidative stress, This suggests that parental behaviour conforms
depletion of carotenoid reserves, or glucocorticoid well to the assumptions of quantitative genetics (i.e.
stress response (Chapter 3). Hormones in partic- that traits are affected by many genes, each with
ular provide important mechanistic links between small effects on phenotype; Chapters 14 and 16).
resource availability and parental care (Chapter 3). Much of the recent excitement in the field of
For example, low levels of glucocorticoid are nec- the molecular genetics of parental care involves
essary for normal metabolism, but glucocorticoid epigenetics. Epigenetics includes post-translational
secretion is triggered when lipid reserves are changes to histone proteins, around which the
exhausted, thereby stimulating glucogenesis and DNA in the cell nucleus is wrapped, and the DNA
protein breakdown to increase energy production itself, for example by methylation (i.e. the addi-
and inducing the cessation of reproduction (i.e. tion of methyl groups; Chapter 17). Methylation
clutch or brood desertion; Wingfield and Sapolsky affects the way in which histones and DNA inter-
2003). The glucocorticoid threshold leading to off- act or the extent to which DNA is transcribed,
spring desertion appears to be modified accord- both of which are central to cellular differentia-
ing to the trade-off between current and future tion. Such epigenetic modifications are important
reproduction, at least in birds, and a recent com- because these changes are often stable, and can
parative analysis shows that species with current be mitotically heritable or inherited across gener-
broods of higher reproductive value had weaker ations (Chapter 17). Environmentally induced epi-
acute stress responses and were less likely to desert genetic changes to DNA can therefore affect the
when exposed to stressors (Bokony et al. 2009). co-evolutionary dynamics of parents and offspring
across generations (Chapter 14). For example, post-
natal maternal grooming in rats induces long-term
18.6.2 Genetic mechanisms
changes in neuro-endocrine function and behaviour
Studies of the molecular genetic mechanisms of offspring, with the variation in the expression
underlying parental care are currently limited to of the genes involved maintained through alter-
a small number of model systems with well- ations in the pattern of DNA methylation (Weaver
characterized genomes, such as honeybees and et al. 2004). Thus, epigenetic variation in parent–
rodents (Chapter 17). In these species, the use of offspring interactions can be modified and deter-
transgenic animals or techniques to alter patterns mined by environmental input such as the level
of gene expression have helped identify candidate of parental care received (Chapter 17). There is
genes that are important in parental care. For exam- also some evidence for transgenerational effects on
ple, in one study on mice, the Sry gene was removed offspring, as rats that experienced relatively lit-
from the Y chromosome (the testes determining fac- tle maternal grooming during development had
tor) and reinserted on an autosome so that gonadal reduced expression of estrogen receptors, mak-
sex determination was independent of the sex chro- ing these females less estrogen sensitive as adults
mosome combination in the transgenic animals (Champagne et al. 2003). Such epigenetic effects on
(Gatewood et al. 2006). Males with an XX comple- parent–offspring interactions that are maintained
ment of chromosomes were less likely to kill young across generations are intriguing because observed
than XY males, whereas XY females were less atten- heritable variation in parent and offspring strate-
tive parents than XX females, indicating that genes gies are potentially both a cause and an effect of
on the Y chromosome are associated with inhibition variable outcomes of parent–offspring interactions.
of parental care (Chapter 17). Studies on sequence Epigenetic signatures may therefore ultimately
variation at particular loci and their relation with determine how strategies are passed on from one
parental care often find that, compared to environ- generation to the next and how heritable variation
mental influences, the per-locus phenotypic effects is maintained. At present the evidence in support
are relatively small (explaining a few per cent of of such a conclusion is based on only a handful
of model systems and the wider prevalence of epi- In cooperatively breeding species, care of offspring
genetic inheritance remains to be further explored. is provided by other members of the group called
The rapidly reducing costs of molecular genetics ‘helpers’ in addition to the parents (see Section
tools means that there is sure to be an explosion of 18.4.2). The helpers retain the ability to reproduce,
work in this field over the next 5–10 years. either currently or in the future, but are suppressed
from breeding by the dominant individuals in the
group (i.e. the breeders; Chapter 12). Typically, such
18.7 Evolutionary implications
groups form when mature offspring delay dispersal
of parental care
and remain on their natal territories to help rear
Co-evolution and correlated responses mean that subsequent broods (Chapter 12). This delayed dis-
selection on parental care traits has important persal is associated with intense competition for
implications for the evolution of other traits and suitable breeding habitat, which means that cooper-
processes. Here we briefly outline some of the con- ation evolves via the effect of ecological constraints
sequences of this co-evolution. on kin structure (Chapter 12). For helpers, staying
on the natal territory to assist in rearing their sib-
lings may therefore represent the ‘best of a bad
18.7.1 Life-history evolution
job’, and there is still considerable scope for conflict
There is considerable variation in life-histories among family members over the provisioning of
among species. Some organisms develop very care (Chapter 12).
quickly, whilst others are slow developers. Some The most derived form of sociality is eusocial-
reproduce just once in a lifetime, producing a large ity, where suppression of reproduction has evolved
number of offspring in a ‘big bang’ (semelparity), from reproductive skew to such an extent that
whilst others produce offspring singly or in batches helpers have lost the ability to mate and repro-
over multiple reproductive events (iteroparity). duce and have become specialized care-givers
Such life-history variation affects the probability (‘workers’). Eusociality is found in some insects,
of the evolution of parental care (Chapter 2), but including some species of bees (e.g. the honeybee
co-evolution means that there is also considerable Apis mellifera), wasps, ants, termites, and also—
scope for parental care, and associated conflicts the only known vertebrate systems—the naked
of interest, to affect the evolution of life-history mole rat Heterocephalus glaber and the Damara-
traits. For example, comparative analyses indicate land mole rat Fukomys damarensis. Eusociality can
that competitive interactions among family mem- evolve from species with parental care via coopera-
bers are associated with parentage and the evo- tive breeding. Such an evolutionary transition can
lution of parent–offspring communication (Briskie only have evolved from a form of care that can
et al. 1994), and with variation in pre- and post-natal be provided by non-breeding adults (e.g. progres-
growth rates in birds (Royle et al. 1999; Lloyd and sive provisioning). In addition, care-giving must
Martin 2003). In addition, models show that sexual be able to be uncoupled from mating and repro-
conflict is expected to lead to the co-evolution of duction. Despite this uncoupling of mating and
biparental care and brood size. This is because the care-giving behaviours, relatedness and patterns of
larger the brood size the more valuable the male’s parentage still play a key role in explaining the
care is to the female (Smith and Härdling 2000). evolution of social complexity (Chapter 11). For
Biparental care can therefore lead to an increase in example, a comparative analysis by Hughes et al.
the number, but not necessarily the quality, of off- (2008) shows that low levels of promiscuity pre-
spring raised (Royle et al. 2006). dict the origin of eusociality in insects. Similarly,
a recent meta-analysis of cooperative breeding in
birds indicates that it is associated with low levels
18.7.2 Social evolution
of extra-group paternity (Cornwallis et al. 2010).
Parental care is also an important evolutionary tran- Consequently, relatedness asymmetries and genetic
sition in the formation of complex social societies. conflicts shape the evolution of complex social
systems much as they shape the evolution of fore emerge and be maintained via a combina-
parental care. tion of sexual selection and co-adaptation between
behavioural development and parental care in fam-
ilies (Roulin et al. 2010).
18.7.3 Sexual selection
Mate choice may be an important driver of the evo-
18.8 Future directions
lution of parental care that has implications for the
evolution of signals of parenting ability in particu- Hamilton (1964) emphasized that it is association
lar (Kvarnemo 2010). If offspring fitness is depen- rather than relatedness per se that is critical to the
dent upon male parental investment, for example, evolution of altruistic behaviour. Parental care is
and there is variation among males in the amount an altruistic behaviour as there is a cost to par-
of care that they provide, then selection is expected ents of providing care but benefits to offspring of
to favour female choice for male sexual ornaments receiving care (Chapter 1). The importance of asso-
that indicate male parental skills (Hoelzer 1989). ciation for the evolution of parental care can be
Males cannot actively demonstrate parenting skills seen by the fact that most species of animal show
at the time of mating, so there should be sex- no parent-offspring association despite having sim-
ual selection for indirect, but reliable, indicators ilarly high relatedness between parents and off-
of parental ability (Candolin 2000). This may be a spring as species with extensive parent-offspring
visual trait, such as the nuptial colouration of male association. These associations are important, not
sticklebacks Gasteroseus aculeatus, or a behavioural only in explaining the evolutionary origins of care
trait or suite of traits, such as personality. (Chapters 1 and 2), but also in explaining the main-
tenance and subsequent evolution of parental care
and complex societies. Parent–offspring associa-
18.7.4 Evolution of personality
tions lead to interactions among individuals, which
Consistent individual differences in behaviour in turn are central to understanding the evolution of
across contexts (also known as ‘personality’) are parental care. There is increasing realization that the
common in non-human animals (Dall et al. 2004). interactions themselves may be as important as the
Such consistency may be advantageous if it con- individuals involved in the interactions, but they
tributes to individual variation in productivity (Biro are closely intertwined. The phenotype (and geno-
and Stamps 2008). However, there is considerable type) of individuals affects how and whom they
variation in the consistency of behaviour of parents interact with, and is an important determinant of
when providing care (Royle et al. 2010). The key to the outcome of conflicts over care. The outcome of
understanding this variation in behaviour, which these interactions among individuals in turn may
is an important determinant of how conflicts are affect the inheritance of phenotypes across genera-
resolved (Chapters 7–9), centres on reliable signals tions through epigenetic effects. Parental traits co-
of parental ability and the co-evolution of parent– evolve with traits in offspring (e.g. provisioning
offspring interactions with behaviours expressed in and begging; Chapters 7, 15, and 16), with other
other functional contexts. Personality may provide parental traits (e.g. paternity and parental care;
a means to reliably indicate parental ability dur- Chapters 6 and 11) and traits expressed in other
ing mate choice, and reduce sexual conflict over species (e.g. social parasites; Chapter 13). The recog-
care, with variation in personalities maintained nition of the importance of the social interactions
by frequency-dependent selection on ‘trustworthi- themselves to the evolution of parental traits is
ness’ (Royle et al. 2010). Furthermore, because fam- possibly the biggest conceptual advance in studies
ily conflicts impose selection on parental and off- of parental care since the publication of Clutton-
spring behaviours via co-adaptation, personality is Brock’s (1991) book, and the recent availability of
expected to co-evolve with patterns of communica- molecular tools that are opening up new avenues of
tion and conflict resolution within families (Roulin research into the genetic and physiological mecha-
et al. 2010). Variation in personality could there- nisms underlying parental care behaviours provide
the likely biggest practical advance (Chapters 3 and evolutionary conflicts over time (Chapter 7), and
17, Section 18.6.2). We outline some of the key areas thereby significantly increase our understanding
for future research below. of the evolutionary origins of parental care traits
The balance between cooperation and conflict: Evolu- (Chapter 4). For example, a recent study proposes
tionary conflicts underlie most, if not all, parental that transposons (‘jumping genes’; Lynch et al.
care traits, limiting the scope for cooperation. How- 2011) were important in the evolutionary origin of
ever, parental care nevertheless involves coopera- viviparity and placentation, which raises intriguing
tion within families (e.g. between male and female new questions about the evolutionary origin of this
parents in biparental care or among sibling ‘helpers’ form of parental care because transposons show
in cooperatively breeding vertebrates), so cooper- very different evolutionary dynamics to regular
ative outcomes are clearly possible. Mechanisms loci. Furthermore, quantitative genetic approaches
facilitating cooperation include behavioural coor- continue to be important in order to understand
dination as a form of reciprocity (Johnstone et al. how genetic covariance can change evolutionary
submitted; Chapter 9), negotiation (e.g. sibling trajectories and zones of conflict (Chapter 16) or
negotiation when resources provided by parents to test hypotheses about patterns of inheritance
are indivisible; Chapter 8) and intergroup conflict of parental care and offspring development and
(facilitating intragroup cooperation; e.g. Bowles behaviour across generations. Finally, compared
2008). These mechanisms work by reducing the dif- to other evolutionary approaches, selection lines
ferential between the fitness optima of family mem- have been little used in the study of the evolution
bers and most research has focused on the study of of parental care, but in order to examine the
these mechanisms. However, we still have a very co-evolution of traits such as paternity and parental
limited understanding of the conflict battleground care (Chapters 6, 9, and 11) they are likely to prove
and it is also possible that individual fitness optima invaluable (Alonzo 2010). In addition we currently
remain divergent but conflict is resolved at little know very little about the quantitative genetics of
or no cost (Cant 2012; Chapter 12). Unlike most physiological mechanisms associated with parental
models of evolutionary conflict, which assume that care (Chapter 3).
an individual’s success depends on how much it Proximate mechanisms underlying parental care: In
invests into competition, this model allows individ- species with parental care a full understanding
uals to either invest in competition or not (Cant of the evolutionary development of an organ-
2012). This mirrors the situation in many coop- ism requires knowledge of how parental care
erative societies, where one class of individuals interacts with offspring development. Technolog-
(e.g. dominants) engage in competitive behaviour ical advances in molecular genetics are likely to
whilst others do not (i.e. subordinates; Chapter contribute particularly to this understanding, espe-
12). However, mechanisms for reducing the costs cially with regard to work on the control of mech-
of conflict whereby some classes of individuals anisms (Chapter 3), but there are numerous other
choose not to compete are not likely to be restricted unresolved issues. These include the role of horme-
to cooperatively breeding species. More empirical sis (or tipping points) in the regulation of parental
work examining cooperative outcomes in the con- care behaviours (Chapters 3 and 6), the physiologi-
text of high potential for conflict (e.g. coordina- cal factors underlying sib–sib interactions (Chapter
tion of begging behaviour towards parents by sib- 8), the hormonal mechanisms regulating behaviour
lings) and conflict in the context of cooperative in cooperatively breeding species (Chapter 12), and
breeding (e.g. suppression of reproduction by dom- the mechanisms involved in adjustments of sex
inants to subordinates) would be insightful in this ratios (Chapter 10). In addition, although models
regard. make explicit assumptions about the shape of fit-
Genetics underlying parental care: More ness functions there is still very little empirical work
widespread availability of sequenced genomes to support these assumptions, despite the shape of
or transcriptomes across species would facilitate fitness functions having profound effects on pre-
comparative studies examining the dynamics of dicted levels of conflict (Mock and Parker 1997;
Chapter 9) and resource allocation decisions such now necessary to bridge the gap between quanti-
as sex ratio adjustment (Chapter 10). The costs and tative genetic and behavioural ecology approaches
benefits of parental care are often difficult to estab- to parental care (e.g. BRNs; Chapters 7 and 16).
lish due to the common currency problem (Chap- Specifically more studies are required that assess
ter 3), but taking a more mechanistic approach the nature of behavioural mechanisms involved in
may help illuminate this issue. Understanding the the negotiation of resources among family mem-
proximate basis of costs and benefits of care is bers, and the factors that select for task special-
also likely to be important in understanding down- ization and its plasticity (Chapter 9). This will
stream effects. help increase our understanding of the behavioural
Downstream effects: Parental care can be con- mechanisms that stabilize biparental care and coop-
sidered an early life-history effect in that the erative breeding systems, and more generally, the
(social) environmental conditions experienced dur- family as a multidimensional social network (Box
ing growth and development when cared for by 18.1). Behavioural plasticity may also be an impor-
parents can have substantial, long-term, effects on tant determinant of success in brood parasites relat-
the phenotype of offspring when adults (Chapters ing to their virulence—an area of research that is
3, 14–16). Despite an upsurge of recent work on currently under-explored (Chapter 13).
parental effects (Chapter 14), including epigenetics Theory: Closer connections between theory and
(Chapters 14 and 17), there are still key areas we empirical work are undoubtedly needed to develop
know very little about. These include downstream models that predict the complex inter-relations
effects of competition early in life (Chapter 8), of among interacting individuals and traits during the
receiving care predominantly from helpers or work- provision of parental care (Chapter 11). In addi-
ers rather than parents (Chapter 12) and the general tion, it is important for models of the evolution of
importance of indirect genetic effects (Chapter 15), sex roles and parental care to explicitly incorporate
and social epistasis (Chapter 16) early in life on the feedback between ecology and the evolution of pat-
expression of traits in adulthood. Understanding terns of parental care (Chapters 2, 6, 9, and 11), and
variation in downstream effects involves an under- for models to clearly distinguish between origins
standing of early life conditions, and, in particular, and maintenance of parental care (Chapter 2). But
the plasticity of behaviour expressed by both par- perhaps the greatest insights will come from the
ents and offspring. Thus, developmental pathways incorporation of parent–offspring trait covariation
in species with parental care cannot be fully under- to models of conflict resolution and more explicit
stood outside the context of parental care, where consideration of how family members interact with
phenotypic and/or genotypic accommodation of one another during the provision of parental care.
parental care and offspring development and their Conflict resolution models address evolutionarily
co-adaptation are expected to shape parental care stable outcomes for parent–offspring interactions,
trait expression and co-evolution. but are currently limited in two different ways.
Plasticity of behaviour: There is considerable vari- They assume that there is no covariation between
ation among individuals in plasticity of behaviour parent and offspring traits and focus on the stable
in the context of parental care. The behavioural sta- co-evolutionary endpoint (Chapter 16). We there-
bility of parent–offspring interactions may depend fore have poor understanding of the evolutionary
on the responsiveness of each of the parties to each origin of offspring influences on parental care and
other (Chapters 7 and 16), which can be a source the co-evolutionary dynamics of parent–offspring
of phenotypic novelties upon which selection can interactions (Chapters 15 and 16). Furthermore,
act (Chapter 14). However, at the other end of the evolutionary models of parent–offspring interac-
spectrum, behavioural consistency may be impor- tions in general assume that interactions between
tant in the context of sexual selection and the res- individuals involve multiple dyadic encounters
olution of sexual conflicts (Royle et al. 2010). More rather than considering all interactions among indi-
studies on the plasticity of parental strategies that viduals simultaneously (i.e. dyads, not networks, of
account for individual variation in behaviour are interactions; Box 18.1). A complete theory of fam-
ily interactions and the evolution of parental care References

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The evolution of parental care: summary, conclusions, and implications

Chapter · August 2012

Nick Royle Per T Smiseth

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The evolution of parental care:

parental interest in the larvae wanes and the rapidly

Sperm Increased mating

Male-biased Positive or Female-biased

Box 18.1 Social networks in the context of parental care

Box 18.1 (Continued)

18.6 Mechanisms and constraints to some extent by introducing state variables

ily interactions and the evolution of parental care References

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