Article

Signals in family conflicts

Abstract and Figures

Although the role of animal signals in the resolution of family conflicts has been thoroughly studied, it has been typically analysed in isolated two-player interactions. For instance, parents are usually considered as the sole receivers of offspring begging signals or mates the receivers of sexual displays. However, this view does not wholly encompass the dynamic and complex nature of the family scenario. In this essay, we review for the first time the clearest evidence of animal signals found to play a role in more than one family context (e.g. mateemate, parenteoffspring and sibesib interactions). We then argue that these signals might have coevolved in multiple family contexts because the whole network of related individuals shares genes and similar physiological mechanisms underlying signal expression and perception abilities. Finally, we propose candidate traits that we would expect to function in multiple family contexts and we consider questions that could be addressed in further studies to understand better the evolution of family signals.
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Essay
Signals in family conicts
Judith Morales
a
,
*
, Alberto Velando
b
a
Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales (CSIC), Madrid, Spain
b
Departamento de Ecoloxía e Bioloxía Animal, Universidade de Vigo, Vigo, Spain
article info
Article history:
Received 12 July 2012
Initial acceptance 8 August 2012
Final acceptance 21 March 2013
Available online 16 May 2013
MS. number: 12-00534R
Keywords:
coevolution
information
manipulation
negotiation
parental care
parenteoffspring conict
sexual conict
sexual imprinting
sexual signal
sibling conict
Although the role of animal signals in the resolution of family conicts has been thoroughly studied, it
has been typically analysed in isolated two-player interactions. For instance, parents are usually
considered as the sole receivers of offspring begging signals or mates the receivers of sexual displays.
However, this view does not wholly encompass the dynamic and complex nature of the family scenario.
In this essay, we review for the rst time the clearest evidence of animal signals found to play a role in
more than one family context (e.g. mateemate, parenteoffspring and sibesib interactions). We then
argue that these signals might have coevolved in multiple family contexts because the whole network of
related individuals shares genes and similar physiological mechanisms underlying signal expression and
perception abilities. Finally, we propose candidate traits that we would expect to function in multiple
family contexts and we consider questions that could be addressed in further studies to understand
better the evolution of family signals.
Ó2013 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
In animal societies, including humans, information exchange
helps researchers understand the interactions among group
members (reviewed in Carazo & Font 2010;Seyfarth et al. 2010;
Ruxton & Schaefer 2011). Learning how individuals use social in-
formation for their common and private interests is one of the keys
to answering outstanding questions in evolutionary biology, such
as the origin of sociality (Danchin & Wagner 1997) and cooperation
(Axelrod & Hamilton 1981). The information that individuals gather
from others modulates tness-related decisions such as where to
live, what to eat and with whom to interact (Danchin et al. 2004).
For instance, information on opponentscondition determines
dominance hierarchies during conicts (e.g. Huntingford &
deLeaniz 1997) and may mitigate the costs of agonistic in-
teractions (Logue et al. 2010). On the other hand, because in-
dividuals need to receive information from conspecics, they
simultaneously make themselves vulnerable to manipulation that
may cause them to deviate from their optimum behaviour (Rice &
Holland 1997). Hence, both information exchange and manipula-
tion can inuence the outcome of social interactions and conict
resolution in societies (Kilner & Hinde 2008).
Interactions among family members are some of the most
common and basic social behaviours exhibited by animals. Family
members constitute a small society with overlapping but not
identical genetic interests, which have been identied as three
main forms of evolutionary conict. Each offspring is more closely
related to itself than to its parents and siblings. Therefore, optimal
parental investment levels for offspring are greater than for parents
(parenteoffspring conict;Trivers 1974). Individual offspring in
turn value their own wellbeing more highly than that of their sib-
lings and thus should try to take a disproportionate share of food
(sibling conict;OConnor 1978). Finally, each parent would prot
if the other provided more care (sexual conict;Lessells 1999).
Given that all family members coincide in time and space to adjust
their decision rules over the same resource (i.e. parental care), all
possible conicts can take place at the same time and thus they
should be analysed simultaneously, as previously proposed by
Parker et al. (2002). However, as a model of social relationships,
intrafamily interactions (parenteoffspring, sibling and mateemate
interactions) have been traditionally studied as isolated events,
either theoretically or empirically (but see Parker 1985;Hinde &
*Correspondence: J. Morales, Departamento de Ecología Evolutiva, Museo
Nacional de Ciencias Naturales (CSIC), c/José Gutiérrez Abascal 2, 28006 Madrid,
Spain.
E-mail address: jmorales@mncn.csic.es (J. Morales).
Contents lists available at SciVerse ScienceDirect
Animal Behaviour
journal homepage: www.elsevier.com/locate/anbehav
0003-3472/$38.00 Ó2013 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.anbehav.2013.04.001
Animal Behaviour 86 (2013) 11e16
Kilner 2007). This prevailing approach has proven highly produc-
tive in many respects, but has also fostered a limited and overly
simplistic view of the complex and dynamic nature of the family
arena.
Analysing intrafamily interactions simultaneously may result in a
more complete view of the mechanisms that underlie conict reso-
lution, such as the use of signals among family members (Godfray &
Johnstone 2000). As in other social contexts, signals may serve to
exchange information between individuals. For instance, sexual
displays can inform mates about the direct or indirect genetic ben-
ets they would accrue by increasing current parental investment
(Burley 1986), and offspring begging signalsmay convey information
to parents about offspringneed or qualityand thus about the benets
of giving extrafood (Godfray 1991;Mock et al. 2011). However, sexual
displays are usually thought to have evolved solely in the context of
sexual selection and begging signals in the parenteoffspring conict.
Yet, could these signals be involved in other family contexts as well?
To answer this question, we rst need to know whether there is ev-
idence that signalling behaviours affect all family members. In fact,
signals are built on the multitude of sensory capacities and neuro-
endocrine responses previously present in the organism and already
established through strong selection (West-Eberhard 1984), and
these pre-existing sensory biases areprobably the same in mates and
offspring and may lead to similarresponses (see, for instance, studies
on human facial neoteny: Jones et al. 1995; on females imitating
begging behaviour of chicks in birds: Tinbergen 1959).
It is widely accepted that most animal communication has
evolved in the context of a network environment (i.e. several sig-
nallers and receivers within communication range of each other;
McGregor 2005). For instance, it has long been recognized that so-
called sexual signalscan function in many social contexts other
than intrasexual or intersexual competition for mates (West-
Eberhard 1983). Still, this broadly accepted complexity of signal-
ling dynamics has rarely been applied to the particular case of the
family, where, as in broader social networks, related individuals
(but also unrelated ones; e.g. the mates) communicate within
transmission range of each others signals (Fig. 1). Whether signals
expressed by family members can be used in multiple family con-
icts remains an open question in most species studied to date.
In this essay, we aim to expand early ideas on the role of signals
in multiple family contexts (Parker et al. 2002). First, we review the
clearest evidence that signalling behaviours affect all family
members. Then we analyse the informative or manipulative func-
tion of these signals as a mechanism for multiple conict resolu-
tion. To conclude, we argue that family signals and the processes
leading to signal expression are only partly captured by a single
family conict and can be best understood in the light of complex
interactions among family members.
SIGNALS THAT WORK IN MULTIPLE FAMILY CONTEXTS
Offspring Begging Signals
The main mechanisms proposed for the resolution of parente
offspring conict (honest signalling and scramble competition
mechanisms) assume that begging displays are directed at parents.
A common prediction of these models is that the probability of
receiving food from parents is proportional to the strength of
begging stimuli (Mock & Parker 1997;Royle et al. 2002), which has
been amply veried in various taxa (e.g. in insects: Smiseth &
Moore 2002; in birds: Leonard et al. 2003). However, very few
studies have broadened this traditional perspective of a dyadic
signalling system (from one nestling to the parent) and explored
the extent to which offspring adjust signalling levels to each other
(Horn & Leonard 2005).
Studies in the barn owl, Tyto alba, suggest that siblings exchange
begging signals in the absence of parents to inform each other
about their need and to negotiatethe levels at which they will beg
when parents arrive at the nest (sibling negotiation hypothesis;
Roulin et al. 2000). Thus, begging signals in the barn owl play a
simultaneous role in the parenteoffspring and sibling conicts
(Table 1). The idea that begging displays have multiple receivers
may explain why offspring sometimes beg in the absence of par-
ents, a behaviour that would otherwise be interpreted as costly and
nonadaptive. Sibling negotiation calls also seem to be characteristic
of the spotless starling, Sturnus unicolor, although in this case
parent-absent begging calls are acoustically distinct from begging
signals directed at parents (Bulmer et al. 2008).
Similarly, the begging behaviour of great tit, Parus major, nes-
tlings not only affects parental feeding rates (Kölliker et al. 1998,
2000), but also the social network structure of nestlings (i.e. the
brood mean strength of associations among nestlings; Royle et al.
2012)(Table 1).
Also in mammals, banded mongoose, Mungos mungo, offspring
increase their begging rates when the background level of begging
by littermates is experimentally lowered (Bell 2007). Additionally,
helpers (escorts) are inuenced by the total begging signal pro-
duced by a litter (Bell 2007). Therefore, in this communally
breeding system begging signals function in both the helpere
offspring and sibling conicts (Table 1).
Parental Signals
As already mentioned, the role of sexual displaysis often
considered solely in mateemate interactions, either before or after
pairing. However, studies on the burying beetle, Nicrophorus ves-
pilloides, reveal that these signals can also be involved in the
parenteoffspring conict. This is one of the rare cases in the
Coleoptera with biparental care and food provisioning to individual
offspring, two important sources of intrafamily conict (reviewed
Male parent
Family signals
Offspring Offspring
Female parent
Helpers
Helpers
Figure 1. Traditionally, family signals have been studied solely in dyadic interactions
among family members (i.e. male parentefemale parent, parenteoffspring and sibesib
interactions). However, given that family members share genes and probably similar
physiological mechanisms underlying signal expression and perception abilities, sig-
nals can simultaneously affect the interactions among all family members. The family
can thus be viewed as a network of related individuals that communicate within
transmission range of each others signals. Modied from Parker et al. 2002 with
permission from the Royal Society.
J. Morales, A. Velando / Animal Behaviour 86 (2013) 11e1612
in Mas & Kölliker 2008). Burying beetles are social insects that base
their mating preferences on cuticular hydrocarbon proles (Steiger
et al. 2008). After mating, a male and a female beetle normally
cooperate to raise their young on small vertebrate carcasses. They
provide care by provisioning the larvae with predigested carrion
and by defending the carcass from the frequent attacks by intruders
(Scott 1998). The mechanism that allows a carcass owner to
discriminate between its original mate and an intruder is based on
the recognition of cuticular hydrocarbon proles (Steiger et al.
2007). Moreover, it has been suggested that the conict of inter-
est between males and females over the duration of parental care is
likely to be hormonally mediated (Scott 1998). Males, which are
expected to benet more than females from early desertion of the
brood, are probably less likely to desert the brood when certain
pheromones are present (Scott 1998). Remarkably, the cuticular
hydrocarbons produced by N. vespilloides parents trigger larval
begging and allow for larval kin discrimination (Smiseth et al.
2010). If the same hydrocarbon proles were used in these
different contexts, studies performed with this species would
provide the rst experimental evidence that a signal used in matee
mate interactions plays a role in the parenteoffspring conict over
care (Table 1).
In birds, there is another suggestive example. However, in this
case, a signal expressed by the parents was rst proposed to
function in the parenteoffspring conict and thereafter (more than
50 years later) in the sexual conict over care. In his pioneering
work, Tinbergen suggested that the red spot on the bill of herring
gull, Larus argentatus, parents stimulates innate begging responses
in newly hatched chicks (Tinbergen & Perdeck 1950), a classic
example in behavioural studies. Notably, in the closely related
yellow-legged gull, Larus cachinnans, the red spot plays a role in the
sexual conict over care, since mates of spot-enlarged parents in-
crease food provisioning to offspring relative to controls (Morales
et al. 2009). Moreover, in this species chicks beg more intensely
when presented with an adult head dummy with an enlarged red
spot (Velando et al. 2013). Overall, these results indicate that the
gulls red spot functions simultaneously in the sexual and the
parenteoffspring conicts (Table 1).
In mammals, the urine of house mice, Mus musculus domesticus,
contains signalling proteins that affect mating preferences in both
sexes (Lin et al. 2005;Swaney et al. 2008). Moreover, the odour of
urine produced by the male and female parents inuences the rate
of ultrasonic vocalizations in pups (Santucci et al. 1994;Kapusta &
Szentgyorgyi 2004). These high-frequency signals are produced by
pups when they are placed outside the nest and they induce
retrieving behaviours in mothers (reviewed in Kölliker & Richner
2001). As in the examples in insects and birds given above, urine
pheromones in mammals represent candidate signals with a
function in both the sexual and the parenteoffspring conicts
(Table 1).
Complex Family: Chemical Signals in Eusocial Insects
Social insects have been proposed as the best experimental
systems for understanding the ancestral conditions for the evolu-
tion of family signals (Mas & Kölliker 2008). In particular, our un-
derstanding of chemical signals in a family network is best
provided through eusocial insects, whose organization in colonies
is determined primarily by pheromones that are actively produced
by the queen, the workers at various tasks and life stages and by the
brood (Slessor et al. 2005). Kin selection predicts a conict between
the queen and her worker daughters over reproduction. Also,
although workers and female larvae are usually more genetically
related than parents and offspring (owing to the haplodiploid
reproductive system), there is potential conict over care between
them. Each larva obtains greater inclusive tness by developing as a
queen than as a worker (Ratnieks et al. 2006). In the honeybee, Apis
mellifera, it is known that components of the queen mandibular
pheromone attract drones, stimulate workers to form the retinue,
to rear brood and to forage for food, and, more importantly, they
suppress the development of workersovaries and thus their
reproductive capacity (reviewed in Slessor et al. 2005). The latter
shows that queen mandibular signals have a profound inuence in
the workerequeen conict over reproduction, but also indirectly in
the workerelarvae conict (Table 1). In this haplodiploid system,
males only transfer genes to the female (diploid) offspring and thus
Table 1
Clearest empirical evidence of animal signals that play a simultaneous role in various family conicts
Species Trait Sender Receiver Family conict Response variable Source
Insects
Burying beetle Chemical signals Parents Offspring Parenteoffspring Begging Smiseth et al. 2010
Nicrophorus
vespilloides
(cuticular
hydrocarbons)
Mates Sexual Male mate choice Steiger et al. 2007
Honeybee
Apis mellifera
Chemical signals
(mandibular
pheromone)
Queen Worker Workerequeen,
Workerelarvae
Worker development
and behaviour
Slessor et al. 2005
Drones Sexual? Attraction Gary 1962
Birds
Herring gull Red spot Parents Offspring Parenteoffspring Begging Tinbergen & Perdeck 1950
Larus argentatus Mates? Sexual?
Yellow-legged gull Red spot Parents Offspring Parenteoffspring Begging Velando et al. 2013
Larus cachinnans Mates Sexual Mate parental care Morales et al. 2009
Barn owl Begging (parents
absent)
Offspring Parents Parenteoffspring Parental care Dreiss et al. 2010
Tyto alba Siblings Sibling Begging (parents present) Roulin et al. 2000;Dreiss et al. 2010
Great tit
Parus major
Begging Offspring Parents Parenteoffspring Parental care Kölliker et al. 1998,2000;Royle et al. 2012
Siblings Sibling Social network structure Royle et al. 2012
Mammals
House mouse
Mus musculus
Chemical signals
(urine odour)
Parents Offspring Parenteoffspring Vocalizations Santucci et al. 1994;Kapusta &
Szentgyorgyi 2004
Mates Sexual Female mate choice
Male mate choice
Lin et al. 2005
Swaney et al. 2008
Banded mongoose
Mungos mungo
Begging Offspring Helper escortHelpereoffspring Parental care Bell 2007
Siblings Sibling Begging
J. Morales, A. Velando / Animal Behaviour 86 (2013) 11e16 13
prefer a female (queen)-biased sex ratio in their offspring, while the
queen prefers an unbiased sex ratio (Baer 2003). Although prob-
able, the role of pheromones in queenemale conict over paternity
and sex ratio remains uncertain.
WHY ARE SIGNALS USED IN SIMULTANEOUS FAMILY
CONTEXTS?
One probable answer is that similar mechanisms underlie
communication among family members. In a family, the nal
outcome of conicts may be negotiatedaccording to the infor-
mation obtained from the opponentssignals or behaviour
(McNamara et al. 1999;Lessells & McNamara 2012). The exibility
of negotiation among family members is partly determined by the
quality of the information on offer (Hinde & Kilner 2007), and the
information is likely to be accessible to all family members and not
only used in dyadic interactions (McGregor 2005). Likewise, sen-
sory biases can be present in all family members and thus manip-
ulative signals may affect multiple family contexts. Both
information exchange and manipulation are likely to inuence the
behavioural rules followed by individuals that are in conict
(Beekman et al. 2003).
In the barn owl example (Table 1), informative negotiation of
resources among siblings has been proposed as a possible solution
of intrabrood conict. The hungrier nestlings invest relatively more
effort in displaying to their rivals, since they are more motivated to
contest the next item delivered when parents arrive. In contrast,
the less hungry nestlings are expected to invest less in displaying to
rivals in order to reduce begging costs (Roulin et al. 2000). Hence,
offspring may gain by advertising their need to one another with
costly begging displays, because this deters the less needy siblings
from competing intensely when a parent arrives at the nest. Owl
parents in turn adjust their provisioning rate to offspring begging
level (Dreiss et al. 2010). Hence, reliable information offered by
begging displays probably underlies multiple family contexts.
Begging intensity in great tits (Table 1) also conveys reliable
information about offspring hunger levels (Kölliker et al. 1998).
Begging intensity is more evenly distributed within broods when
female parents provide more food than male parents, which sug-
gests that parents are not equally responsive to variation in the
information conveyed, that is, hunger levels (Royle et al. 2012).
Moreover, begging behaviour relates to offspring gregariousness,
which in turn predicts family tness (Royle et al. 2012). Thus,
begging signals probably contribute to shaping cooperative
behaviour among family members, enhancing group performance.
Similarly, in the communally breeding banded mongoose (Table 1),
information exchange by means of begging signals may facilitate
cooperation among family members. Each pup forms an exclusive
relationship with a single helper, its escort, but escorts are affected
by begging of the whole brood, favouring cooperation among lit-
termates (Bell 2007). Since all brood mates benet from having
companions, cooperative begging signals potentially offset under-
lying genetic conicts (Bell 2007).
Also, reliable information conveyed by the red spot on the bill
may affect negotiation rules within a family of yellow-legged gulls
(Table 1). Red spot expression is costly for parents to produce and
reects their current antioxidant status (Pérez et al. 2008). Thus,
mates can use this information to evaluate the direct or indirect
benets of their own investment, according to the differential
allocation theory (Burley 1986). It is unknown whether the infor-
mation conveyed by the red spot can also affect parenteoffspring
negotiation rules on the amount of resources allocated to them. It
seems likely, since offspring show a begging preference for larger
red spots (Velando et al. 2013), presumably expressed by high-
quality caregivers. Alternatively, parents could be exploiting a
sensory bias in chicks towards red objects. Begging signals trig-
gered by the adults red spot are costly to produce and inform
parents about the chicks hunger and condition (Noguera et al.
2010). Hence, the red spot expression in the parents might
impose a cost to chicks that prevents begging exaggeration and, in
this case, parents would always winthe conict (Godfray 1991).
Chemical signals may also offer reliable information to other
family members. In the honeybee (Table 1), it has been argued that
the queen pheromones would exibly affect the outcome of
workerequeen conict over reproduction if they were honest sig-
nals of queen fertility and, hence, would inform workers about the
genetic benets they would gain by self-restraint (Keller & Nonacs
1993). Yet, as in the example in gulls given above, it is unresolved
whether parental signals (queen pheromones in the case of the
honeybee) are informative or manipulative. If the signals are
manipulative in the honeybee, the queen would have control and
always win the conict with workers, irrespective of her fertility.
CONCLUSIONS AND PROSPECTS
The examples shown in Table 1 reveal that a given signal can
function simultaneously in various family contexts and that family
members are not conned to dyadic interactions, but rather they
form a dynamic communication network. This perspective suggests
new questions that need to be addressed to understand fully the
evolution of signals in the family arena.
First, signals used in intrafamily interactions act as reciprocal
environmental inuences on the phenotype of other family mem-
bers, and thus they may exert indirect genetic effects on them
(Moore et al. 1997;Kölliker et al. 2012). For instance, the early social
environment of offspring shapes the strategy not only that they
later adopt as parents but also that they transmit to their own
offspring (Meunier & Kölliker 2012). When tness-related traits of
family members inuence each other and are heritable, the
consequence is a correlational selection among these traits (i.e.
social epistasis; Wolf & Brodie 1998). Thus, if sexualsignals in-
uence mate and offspring behaviour, an interesting aspect is that
offspring preferences may also play a role in runaway selection (i.e.
linkage disequilibrium between sexual trait and preferences).
Therefore, they could increase directional selection on sexual traits
when genetic covariance is positive or limit their expression when
covariance is negative (West-Eberhard 1983).
Nevertheless, we should rst explore whether sexually selected
traits that affect offspring behaviour in Table 1 are rare cases or
examples of an overlooked process. We consider that a promising
starting point for further research is to study the role of parental
signals during parenteoffspring interactions in species in which
sexual imprinting has already been demonstrated (such as many
species of fowl, ducks, geese, pigeons and doves, gulls, parrots and
songbirds). In many animals, early exposure of young animals to
parental signals has a dramatic inuence on sexual preferences
when they reach adulthood (e.g. Lorenz 1935;Kendrick et al. 1998;
Penn & Potts 1998;Jacob et al. 2002;Kozak et al. 2011). Hence,
adults base their preferences on the scents, sounds, colours or other
stimuli to which they were inevitably exposed as offspring very
early in their development. This indicates that parental signals
strongly inuence, with a delay, offspring behaviour. But do they
inuence offspring during parenteoffspring interactions as well?
Apart from studies in mammals, which suggest that offspring have
the ability to recognize and select their mothers scent during
development (Yamazaki et al. 2000; reviewed in Brennan &
Kendrick 2006), this question remains practically unexplored.
Another group of candidate traits are those expressed in species
with prolonged and intensive parental care. For instance, in many
seabirds offspring are continuously exposed to conspicuous colours
J. Morales, A. Velando / Animal Behaviour 86 (2013) 11e1614
on the parents bill, gape, eye rings and feet, some of which are
known to play a role in sexual selection (Torres & Velando 2003;
2005) and to reect current parental nutritional quality
(Kristiansen et al. 2006;Velando et al. 2006;Leclaire et al. 2011).
These examples may also help to solve questions on the evolution
of female ornamentation. After mating, one explanation for the
presence of ornaments in the pair bond is that they evolve because
they stimulate the partner to increase parental investment
(Servedio et al. 2013). However, this possibility has been little
explored in females (reviewed in Ratikainen & Kokko 2010). An
additional explanation that would be interesting to test is whether
offspring can be receivers of maternal signals and, in general, of
parental signals in species with intense biparental care.
Second, given that signals are accessible to all family members,
parental care strategies are probably inuenced by the interaction
between signals expressed by different members. For instance,
parental provisioning behaviour in yellow-legged gulls depends on
both the expression of the red spot on the mates bill and offspring
begging signals (Morales et al. 2009). Thus, parental decision rules
are complex because they integrate the information conveyed by
different types of signals in simultaneous family conicts. Further
empirical studies that simultaneously manipulate two different
signals (e.g. signals used in mate attraction and offspring signals)
are required to know how their joint effect inuences the behav-
ioural strategies of all family members.
Third, to understand the type of signals that function in multiple
conicts we also need to determine whether parental allocation is
controlled primarily by parents or by their offspring. Depending on
who controls parental investment, a given signal is likely either to
manipulate or to inform other family members, or both. If parents
control food provisioning, we may expect honest offspring signals
to evolve to convey reliable information about hunger or condition
(Parker et al. 2002). But if parents lack full control of food allocation,
offspring may be expected to use begging signals to manipulate
parental provisioning (Parker et al. 2002), but at the same time to
negotiate with their siblings over who has priority in the following
feeding attempt (Johnstone & Roulin 2003).
Lastly, another issue that remains practically unexplored is
whether parental signals can inuence the decision rules of helpers
in cooperatively breeding vertebrates, as demonstrated in insect
colonies. If there are direct benets of helping (e.g. increased sur-
vival, mating success, ability to rear offspring or chances of suc-
cessful dispersal; Clutton-Brock 2002), nonbreeding individuals
could compete to become helpers. Signals could thus be used to
form dominance hierarchies among relatives (and also among
nonrelatives) that establish an order of participation in cooperative
breeding tasks and access to resources. Exploring the role of signals
during the formation of dominance hierarchies in social organisms
and its effects in the whole family will contribute to explaining how
cooperative breeding is maintained.
We have emphasized that parental investment reects the
simultaneous resolution of multiple family conicts, as previously
proposed by Parker (1985) and Parker et al. (2002). Here we provide
a more detailed development of this idea with a special focus on
signals and the processes leading to their expression. Whatever
their origin, signals are not isolated from other actors and signals in
the family scenario. They might have coevolved in multiple con-
texts within the network of related individuals, because they share
genes and similar physiological mechanisms underlying signal
expression and perception abilities. Given that selection can act on
multiple traits simultaneously, the evolutionary response to se-
lection for parental provisioning should depend on the genetic
covariances between the signalling behaviours of all family mem-
bers (Kölliker et al. 2005). Signals may be selected through the sum
of adaptive responses of family members, although their expression
may also be constrained by maladaptive responses owing to shared
sensory capacities. Future coadaptation models should consider
mateemate as well as parenteoffspring interactions to explore
how parental care can be coadapted because of the combined ef-
fects of these multiple signalling behaviours on tness.
Acknowledgments
We are grateful to three anonymous referees for their helpful
and constructive comments. We thank Angela Turner for linguistic
corrections. J.M. was supported by a contract Junta para la
Ampliación de Estudiosfunded by CSIC and ESF and A.V. by a
project (CGL2009-10883-C02-01) from the former Ministerio de
Innovación y Ciencia.
References
Axelrod, R. & Hamilton, W. D. 1981. The evolution of cooperation. Science,211,
1390e1396.
Baer, B. 2003. Bumblebees as model organisms to study male sexual selection in
social insects. Behavioral Ecology and Sociobiology,54,521e533.
Beekman, M., Komdeur, J. & Ratnieks, F. L. W. 2003. Reproductive conicts in
social animals: who has power? Trends in Ecology & Evolution,18, 277e282.
Bell, M. B. V. 2007. Cooperative begging in banded mongoose pups. Current Biology,
17,717e721.
Brennan, P. A. & Kendrick, K. M. 2006. Mammalian social odours: attraction and
individual recognition. Philosophical Transactions of the Royal Society B,361,
2061e2078.
Bulmer, E., Celis, P. & Gil, D. 2008. Parent-absent begging: evidence for sibling
honesty and cooperation in the spotless starling (Sturnus unicolor). Behavioral
Ecology,19,279e284.
Burley, N. 1986. Sexual selection for aesthetic traits in species with biparental care.
American Naturalist,127,415e445.
Carazo, P. & Font, E. 2010. Putting information back into biological communication.
Journal of Evolutionary Biology,23,661e669.
Clutton-Brock, T. 2002. Breeding together: kin selection and mutualisms in
cooperative vertebrates. Science,296,69e72.
Danchin, E. & Wagner, R. H. 1997. The evolution of coloniality: the emergence of
new perspectives. Trends in Ecology & Evolution,12, 342e347.
Danchin, E., Giraldeau, L. A., Valone, T. J. & Wagner, R. H. 2004. Public informa-
tion: from nosy neighbors to cultural evolution. Science,305, 487e
491.
Dreiss, A., Lahlah, N. & Roulin, A. 2010. How siblings adjust sib-sib communication
and begging signals to each other. Animal Behaviour,80, 1049e1055.
Gary, N. E. 1962. Chemical mating attractants in the queen honey bee. Science,13 6,
773e774.
Godfray, H. C. J. 1991. Signalling of need by offspring to their parents. Nature,352,
328e330.
Godfray, H. C. J. & Johnstone, R. A. 2000. Begging and bleating: the evolution of
parent-offspring signalling. Philosophical Transactions of the Royal Society B,355,
1581e1591.
Hinde, C. A. & Kilner, R. M. 2007. Negotiations within the family over the supply of
parental care. Proceedings of the Royal Society B,274,53e60.
Horn, A. G. & Leonard, M. L. 2005. Nesting begging as a communication network.
In: Animal Communication Networks (Ed. by P. K. McGregor), pp. 170e190.
Cambridge: Cambridge University Press.
Huntingford, F. A. & deLeaniz, C. G. 1997. Social dominance, prior residence and
the acquisition of protable feeding sites in juvenile Atlantic salmon. Journal of
Fish Biology,51,1009e1014.
Jacob, S., McClintock, M. K., Zelano, B. & Ober, C. 2002. Paternally inherited HLA
alleles are associated with womens choice of male odor. Nature Genetics,30,
175 e179.
Johnstone, R. A. & Roulin, A. 2003. Sibling negotiation. Behavioral Ecology,14,
780e786.
Jones, D., Brace, C. L., Jankowiak, W., Laland, K. N. & Musselman, L. E. 1995.
Sexual selection, physical attractiveness, and facial neoteny: cross-cultural ev-
idence and implications. Current Anthropology,36,723e748.
Kapusta, J. & Szentgyorgyi, H. 2004. Ultrasonic responses of CBA pups to the odour
of genetically different mice. Behaviour,141,157e167.
Keller, L. & Nonacs, P. 1993. The role of queen pheromones in social insects: queen
control or queen signal. Animal Behaviour,45, 787e794.
Kendrick, K. M., Hinton, M. R., Atkins, K., Haupt, M. A. & Skinner, J. D. 1998.
Mothers determine sexual preferences. Nature,395, 229e230.
Kilner, R. M. & Hinde, C. A. 2008. Information warfare and parent-offspring con-
ict. Advances in the Study of Behavior,38, 283e336.
Kölliker, M. & Richner, H. 2001. Parent-offspring conict and the genetics of
offspring solicitation and parental response. Animal Behaviour,62, 395e407.
Kölliker, M., Richner, H., Werner, I. & Heeb, P.1998. Begging signals and biparental
care: nestling choice between parental feeding locations. Animal Behaviour,55,
215e222.
J. Morales, A. Velando / Animal Behaviour 86 (2013) 11e16 15
Kölliker, M., Brinkhof, M. W. G., Heeb, P., Fitze, P. S. & Richner, H. 2000. The
quantitative genetic basis of offspring solicitation and parental response in a
passerine bird with biparental care. Proceedings of the Royal Society B,267,
2127e2132.
Kölliker, M., Brodie, E. D., III & Moore, A. J. 2005. The coadaptation of parental
supply and offspring demand. The American Naturalist,16 6, 506e516 .
Kölliker, M., Royle, N. J. & Smiseth, P. T. 2012. Parent-offspring co-adaptation. In:
The Evolution of Parental Care (Ed. by N. J. Royle, P. T. Smiseth & M. Kölliker),
pp. 285e299. Oxford: Oxford University Press.
Kozak, G. M., Head, M. L. & Boughman, J. W. 2011. Sexual imprinting on ecolog-
ically divergent traits leads to sexual isolation in sticklebacks. Proceedings of the
Royal Society B,278, 2604e2610.
Kristiansen, K. O., Bustnes, J. O., Folstad, I. & Helberg, M. 2006. Carotenoid
coloration in great black-backed gull Larus marinus reects individual quality.
Journal of Avian Biology,37,6e12.
Leclaire, S., White, J., Arnoux, E., Faivre, B., Vetter, N., Hatch, S. A. & Danchin, E.
2011. Integument coloration signals reproductive success, heterozygosity, and
antioxidant levels in chick-rearing black-legged kittiwakes. Natur-
wissenschaften,98,773e782.
Leonard, M. L., Horn, A. G. & Parks, E. 2003. The role of posturing and calling
in the begging display of nestling birds. Behavioral Ecology and Sociobiology,
54,188e193.
Lessells, C. M. 1999. Sexual conict. In: Levels of Selection in Evolution (Ed. by
L. Keller), pp. 75e99. Princeton, New Jersey: Princeton University Press.
Lessells, C. M. & McNamara, J. M. 2012. Sexual conict over parental investment in
repeated bouts: negotiation reduces overall care. Proceedings of the Royal Society
B,279, 1506e1514.
Lin, D. Y., Zhang, S. Z., Block, E. & Katz, L. C. 2005. Encoding social signals in the
mouse main olfactory bulb. Nature,434,470e47 7.
Logue, D. M., Abiola, I. O., Rains, D., Bailey, N. W., Zuk, M. & Cade, W. H. 2010.
Does signalling mitigate the cost of agonistic interactions? A test in a cricket
that has lost its song. Proceedings of the Royal Society B,277,2571e2575.
Lorenz, K. 1935. Der Kumpan in der Umwelt des Vogels. Journal of Ornithology,83,
137e213.
McGregor, P. 2005. Animal Communication Networks. Cambridge: Cambridge
University Press.
McNamara, J. M., Gasson, C. E. & Houston, A. I. 1999. Incorporating rules for
responding into evolutionary games. Nature,401, 368e371.
Mas, F. & Kölliker, M. 2008. Maternal care and offspring begging in social insects:
chemical signalling, hormonal regulation and evolution. Animal Behaviour,76,
1121e1131.
Meunier, J. & Kölliker, M. 2012. Parental antagonism and parent-offspring co-
adaptation interact to shape family life. Proceedings of the Royal Society B,279,
3981e3988.
Mock, D. W., Dugas, M. B. & Strickler, S. A. 2011. Honest begging: expanding from
signal of need. Behavioral Ecology,22, 909e917.
Mock, D. W. & Parker, G. A. 1997. The Evolution of Sibling Rivalry. Oxford: Oxford
University Press.
Moore, A. J., Brodie, E. D. & Wolf, J. B. 1997. Interacting phenotypes and the
evolutionary process: I. Direct and indirect genetic effects of social interactions.
Evolution,51,1352e1362.
Morales, J., Alonso-Alvarez, C., Pérez, C., Torres, R., Serano, E. & Velando, A.
2009. Families on the spot: sexual signals inuence parent-offspring in-
teractions. Proceedings of the Royal Society B,276,2477e2483.
Noguera, J. C., Morales, J., Pérez, C. & Velando, A. 2010. On the oxidative cost of
begging: antioxidants enhance vocalizations in gull chicks. Behavioral Ecology,
21,479e484.
OConnor, R. J. 1978. Brood reduction in birds: selection for fratricide, infanticide
and suicide? Animal Behaviour,26,79e96.
Parker, G. A. 1985. Models of parent-offspring conict. V. Effects of the behaviour of
the two parents. Animal Behaviour,33,519e533.
Parker, G. A., Royle, N. J. & Hartley, I. R. 2002. Intrafamilial conict and parental in-
vestment: a synthesis. Philosophical Transactions of the Royal Society B,357,295e307.
Penn, D. & Potts, W. 1998. MHC-disassortative mating preferences reversed by
cross-fostering. Proceedings of the Royal Society B,265, 1299e1306.
Pérez, C., Lores, M. & Velando, A. 2008. The availability of nonpigmentary anti-
oxidant affects red coloration in gulls. Behavioral Ecology,19,967e973.
Ratikainen, I. I. & Kokko, H. 2010. Differential allocation and compensation: who
deserves the silver spoon? Behavioral Ecology,21,195e200.
Ratnieks, F. L. W., Foster, K. R. & Wenseleers, T. 2006. Conict resolution in insect
societies. Annual Review of Entomology,51, 581e608.
Rice, W. R. & Holland, B. 1997. The enemies within: intergenomic conict, inter-
locus contest evolution (ICE) and the intraspecic red queen. Behavioral Ecology
and Sociobiology,41,1e10.
Roulin, A., Kölliker, M. & Richner, H. 2000. Barn owl (Tyto alba) siblings vocally
negotiate resources. Proceedings of the Royal Society B,267, 459e463.
Royle, N. J., Hartley, I. R. & Parker, G. A. 2002. Begging for control: when are
offspring solicitation behaviours honest? Trends in Ecology & Evolution,17,
434e440.
Royle, N. J., Pike, T. W., Heeb, P., Richner, H. & Kölliker, M. 2012. Offspring social
network structure predicts tness in families. Proceedings of the Royal Society B,
279,4914e4992.
Ruxton, G. D. & Schaefer, H. M. 2011. Resolving current disagreements and am-
biguities in the terminology of animal communication. Journal of Evolutionary
Biology,24,2574e2585.
Santucci, D., Masterson, D. & Elwood, R. W. 1994. Effects of age, sex, and odors
from conspecic adult males on ultrasonic vocalizations of infant CS1 mice.
Behavioural Processes,32, 285e295.
Scott, M. P. 1998. The ecology and behavior of burying beetles. Annual Review of
Entomology,34, 367e373.
Servedio, M. R., Price, T. D. & Lande, R. 2013. Evolution of displays within the pair
bond. Proceedings of the Royal Society B,280,1757.
Seyfarth, R. M., Cheney, D. L., Bergman, T., Fischer, J., Zuberbühler, K. &
Hammerschmidt, K. 2010. The central importance of information in studies of
animal communication. Animal Behaviour,80,3e8.
Slessor, K. N., Winston, M. L. & Le Conte, Y. 2005. Pheromone communication in
the honeybee (Apis mellifera L.). Journal of Chemical Ecology,31,2731e2745.
Smiseth, P. T. & Moore, A. J. 2002. Does resource availability affect offspring
begging and parental provisioning in a partially begging species? Animal
Behaviour,63,577e585.
Smiseth, P. T., Andrews, C., Brown, E. & Prentice, P. M. 2010. Chemical stimuli
from parents trigger larval begging in burying beetles. Behavioral Ecology,21,
526e531.
Steiger, S., Peschke, K., Francke, W. & Müller, J. K. 2007. The smell of parents:
breeding status inuences cuticular hydrocarbon pattern in the burying beetle
Nicrophorus vespilloides.Proceedings of the Royal Society B,274,2211e
2220.
Steiger, S., Franz, R., Eggert, A.-K. & Müller, J. K. 2008. The Coolidge effect, indi-
vidual recognition and selection for distinctive cuticular signatures in a burying
beetle. Proceedings of the Royal Society B,275, 1831e1838.
Swaney, W. T., Curley, J. P., Champagne, F. A. & Keverne, E. B. 2008. The paternally
expressed gene Peg3 regulates sexual experience-dependent preferences for
estrous odors. Behavioral Neuroscience,122, 963e973.
Tinbergen, N. 1959. Comparative studies of the behaviour of gulls (Laridae): a
progress report. Behaviour,15,1e70.
Tinbergen, N. & Perdeck, A. C. 1950. On the stimulus situation releasing the
begging response in the newly hatched herring gull chick (Larus argentatus
argentatus Pont.). Behaviour,3,1e39.
Torres, R. & Velando, A. 2003. A dynamic trait affects continuous pair assessment
in the blue-footed booby (Sula nebouxii). Behavioral Ecology and Sociobiology,55,
65e72.
Torres, R. & Velando, A. 2005. Male preference for female foot colour in the socially
monogamous blue-footed booby, Sula nebouxii.Animal Behaviour,69,59e65.
Trivers, R. 1974. Parent-offspring conict. American Zoologist,14, 249e264.
Velando, A., Beamonte-Barrientos, R. & Torres, R. 2006. Pigment-based skin
colour in the blue-footed booby: an honest signal of current condition used by
females to adjust reproductive investment. Oecologia,149, 535e542.
Velando, A., Kim, S.-Y. & Noguera, J. C. 2013. Begging response of gull chicks to the
red spot on the parental bill. Animal Behaviour,85, 1359e1366.
West-Eberhard, M. J. 1983. Sexual selection, social competition, and speciation. The
Quarterly Review of Biology,58,155e183.
West-Eberhard, M. J. 1984. Sexual selection, competitive communication and
species-specic signals in insects. In: Insect Communication (Ed. by T. Lewis),
pp. 283e324. New York: Academic Press.
Wolf, J. B. & Brodie, E. D. 1998. The coadaptation of parental and offspring char-
acters. Evolution,52, 299e308.
Yamazaki, K., Beauchamp, G. K., Curran, M., Bard, J. & Boyse, E. A. 2000. Parent-
progeny recognition as a function of MHC odortype identity. Proceedings of the
National Academy of Sciences, U.S.A.,97, 10500e10502.
J. Morales, A. Velando / Animal Behaviour 86 (2013) 11e1616
... Likewise, the expression of signals of quality can play a role in settling conflicts among relatives in species with parental care (Grodzinski and Johnstone 2012;Morales and Velando 2013). Family members constitute a small society with overlapping but not identical interests (Trivers 1974). ...
... First, social interactions and information exchange are more frequent in large groups (Pacala et al. 1996), and signals (at least, nonmanipulative ones) have evolved to facilitate information exchange and the resolution of social conflicts (for intrafamily conflict see Trivers 1974;Godfray 1995). Second, social networks are probably more complex in large families (Morales and Velando 2013), simply because there is a higher probability of interacting with more individuals. Third, sibling conflict is expected to be stronger in large broods, since the higher the number of young to be fed the stronger the competition for limited parental resources (i.e., intrabrood conflict; Godfray and Parker 1992;Kilner 1999Kilner , 2006Smiseth et al. 2007). ...
... Results also show that juvenile plumage whiteness is more frequent in open-nesting passerines, although this relationship depended on the subset of species included in the analysis. The detected association between clutch size and feather whiteness suggests that selection maintains offspring conspicuousness in large families, perhaps because offspring signals facilitate information exchange in large groups and the resolution of intrafamily conflicts (Morales and Velando 2013). Similarly, mouth and flange color patterns in juvenile birds are more likely to evolve in larger families (Krebs and Putland 2004;Soler and Avilés 2010; but see Kilner and Davies 1998) and when there is a higher degree of intrabrood conflict, due to extrapair paternity or brood reduction (Kilner 1999;Avilés et al. 2008). ...
Article
The offspring of many animals are conspicuous during parental dependence, despite juveniles generally suffering from high predation risk. However, to date, it is unclear whether offspring structural ornaments play a role in intrafamily communication. This is the case of conspicuous plumage in young birds, which is worn unchanged during a long period after fledging, when they still depend on their parents. If plumage color facilitates intrafamily interactions, its role should be more important in large-brooded species, where the strength of intrafamily conflict is potentially stronger. We therefore performed a comparative study in 210 passerine bird species to test whether an offspring structural trait, white plumage, evolves more frequently in lineages with larger clutches. We also explored the number of broods raised per year as another source of intrafamily conflict. First, we found that juvenile whiteness was more frequent in open-nesting species. Moreover, in agreement with our prediction, the presence of juvenile white tail/wing patches was strongly and positively associated with clutch size. This relationship was not due to the strong resemblance between offspring and adult plumage, which was controlled for in the statistical analyses. Moreover, the association remained significant after taking into account predation risk, for which there was information for a subset of species. In contrast, juvenile whiteness was not associated with the number of broods raised per year. These results may suggest that the evolution of juvenile conspicuousness is favored in species with potentially stronger intrabrood sibling conflict.
... Carotenoids are crucial at early stages of development, since they reduce embryonic ROS damage (Surai & Speake, 1998) and enhance offspring immune system before (Surai, Speake, & Sparks, 2001) and after hatching (Haq, Bailey, & Chinnah, 1996;McWhinney, Bailey, & Panigrahy, 1989). Furthermore, they have a positive effect on offspring growth (Biard, Surai, & Møller, 2007) and influence the development of traits like plumage or beak coloration that play an important role in parentoffspring communication (Morales & Velando, 2013;Tschirren, Fitze, & Richner, 2005). ...
... Lutein is a carotenoid pigment included in the group of xanthophylls. Lutein and zeaxanthin are the main carotenoids in bird plasma (>90%; McGraw, 2006) and in bird eggs , and are critical for offspring growth and feather color development (Morales & Velando, 2013;Tschirren et al., 2005). ...
Article
Full-text available
During egg laying, females face a trade‐off between self‐maintenance and investment into current reproduction, since providing eggs with resources is energetically demanding, in particular if females lay one egg per day. However, the costs of egg laying not only relate to energetic requirements, but also depend on the availability of specific resources that are vital for egg production and embryonic development. One of these compounds are carotenoids, pigments with immuno‐stimulatory properties, which are crucial during embryonic development. In this study, we explore how carotenoid availability alleviates this trade‐off and facilitates egg laying in a small bird species, the blue tit (Cyanistes caeruleus). Blue tits have among the largest clutch size of all European passerines and they usually lay one egg per day, although laying interruptions are frequent. We performed a lutein supplementation experiment and measured potential consequences for egg laying capacity and egg quality. We found that lutein‐supplemented females had less laying interruptions and thus completed their clutch faster than control females. No effects of treatment were found on the onset of egg laying or clutch size. Experimentally enhanced carotenoid availability did not elevate yolk carotenoid levels or egg mass, but negatively affected eggshell thickness. Our results provide hence evidence on the limiting role of carotenoids during egg laying. However, the benefits of laying faster following lutein supplementation were counterbalanced by a lower accumulation of calcium in the eggshell. Thus, even though single components may constrain egg laying, it is the combined availability of a range of different resources which ultimately determines egg quality and thus embryonic development.
... However, family members (mates and offspring) usually coincide in time and space, and the information conveyed by signallers can be used by multiple family members simultaneously. Hence, the family is a social environment in which signals can function in multiple contexts (Morales and Velando 2013). To take an example, the size of the red-dot on the bill of the yellow-legged gull, Larus michaellis, affects a mate's parental investment (Morales et al. 2009) and at the same time, it induces chick begging . ...
Article
Full-text available
In bi-parental species, reproduction is not only a crucial life-history stage where individuals must take fitness-related decisions, but these decisions also need to be adjusted to the behavioural strategies of other individuals. Hence, communication is required, which could be facilitated by informative signals. Yet, these signalling traits might have (co-)evolved in multiple contexts, as various family members usually meet and interact during reproduction. In this study, we experimentally explored for the first time whether a colourful plumage trait in adults acts as a signal that regulates multiple intra-family interactions in a bird species, the blue tit ( Cyanistes caeruleus ). We expected that an experimental reduction of adults’ UV/yellow reflectance (i.e. a reduction of apparent individual quality) should affect the behavioural strategies of all family members. We found evidence for this at least in adults, since the partners of UV-blocked individuals (either males or females) increased their parental investment — perhaps to compensate for the apparent lower condition of their mates. As the UV-blocked adult did not change its provisioning behaviour, the partner presumably responded to the manipulated signal and not to a behavioural change. However, the offspring did not co-adjust their begging intensity to the experimental treatment. It is thus possible that they responded to overall parental care rather than the signal. These results suggest that UV/yellow colouration of adult blue tits may act as quality signal revealing the rearing capacity to mates. Significance statement How parents respond to signals of genetic or phenotypic quality of their mates has received significant attention. However, previous studies have primarily focused on the receiver’s response and have not always controlled for the signaller’s behaviour and its investment in reproduction. Our results provide the first experimental evidence that ultraviolet (UV)/yellow colouration acts as a signal of parental quality in the blue tit. Parents responded by increasing their effort when paired with UV-blocked (low-quality) mates, while controlling for the mate’s behaviour. We argue that the reduced expression of the signal triggered a compensatory response in the mate. Interestingly, both males and females responded similarly to changes in mate’s UV/yellow reflectance, suggesting similar rules over investment in response to this trait. However, nestlings, a potential (and often neglected) set of observers of parental signals, did not change their behaviour when raised by an UV-blocked (= low-quality) parent.
... A couple of paradigmatic examples are the tail feathers of male peacocks or male deer antlers, and one main mechanism proposed to ensure the honesty of such signals is that they are costly to produce and maintain (15)(16). Interestingly, however, it is evident that signalling can play a signi cant role in other non-sexual contexts, including the period of parental care (17). Here, both offspring and parents are potential bearers and receivers of signals of quality expressed by other family members (18)(19). ...
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Full-text available
Parents allocate resources to offspring to increase their survival and to maximize their own fitness, while this investment implies costs to their condition and future reproduction. Parents are hence expected to optimally allocate their resources. They should invest equally in all their offspring under good conditions, but when parental capacity is limited, parents should invest in the offspring with the highest probability of survival. Such parental favouritism is facilitated by the fact that offspring have evolved condition-dependent traits to signal their quality to parents. In this study we explore whether the parental response to an offspring quality signal depends on the intrinsic capacity of the parents, here the female. We first manipulated the intrinsic capacity of blue tit ( Cyanistes caeruleus ) females through lutein-supplementation during egg laying, and we subsequently blocked the UV/yellow reflectance of breast feathers on half of the nestlings in each brood. However, we did not find evidence that the female intrinsic capacity shaped parental favouritism for offspring UV/yellow colouration, as there were no differences in parental feeding or sibling competition. However, we found that males were more responsive than females to nestling UV/yellow when rearing capacity was high, as indicated by the prey-testings (when a parent places a prey item into a nestling’s gape but removes it again). Furthermore, when considering a more integrative measure, offspring growth, we did find the expected interaction effect. In control nests, UV-blocked nestlings gained less body mass than their non-UV-blocked siblings, whereas in lutein-supplemented nests UV-blocked nestlings gained more mass than their siblings. Overall, our results emphasize the female’s environment at an early reproduction stage shaped the role of offspring UV/yellow during family interactions illustrating plasticity in parental feeding rules.
... Conflict in avian societies can take many forms and is extremely common (Morales and Velando, 2013). ...
Chapter
Understanding the interaction between cooperation and conflict in establishing effective social behaviour is a fundamental challenge facing societies. Reflecting the breadth of current research in this area, this volume brings together experts from biology to political science to examine the cooperation–conflict interface at multiple levels, from genes to human societies. Exploring both the exciting new directions and the biggest challenges in their fields, the authors focus on identifying commonalities across species and disciplines to help understand what features are shared broadly and what are limited to specific contexts. Each chapter is written to be accessible to students and researchers from interdisciplinary backgrounds, with text boxes explaining terminology and concepts that may not be familiar across disciplinary boundaries, while being a valuable resource to experts in their fields.
... Conflict in avian societies can take many forms and is extremely common (Morales and Velando, 2013). ...
Chapter
The evolutionary paradox of animals helping others in their social group, rather than living independently, has fascinated researchers for many decades. Ultimately, this cooperation is hypothesized to have evolved because the benefits of cooperation outweigh the costs (Hamilton, 1964), and considerable empirical evidence supports this hypothesis (see Koenig and Dickinson, 2016). However, one major cost of cooperation, particularly for territorial cooperative breeders, is conflict (Shen et al., 2017; Nelson-Flower et al., 2018a). This conflict may occur both within and between groups; such conflict includes access to reproductive opportunities, social status, territory, water, or food. We suggest that a consideration of the influence of both intergroup and intragroup levels of conflict in individual decisions to cooperate is essential, since intragroup conflict may lead to decisions to disperse if intergroup opportunities to mate are high, whereas high levels of intergroup conflict may promote intragroup cooperation in order to defend existing resources (see Chapter 10 for review of inter-vs. intragroup aggression in social insects). Conflict is therefore a natural outcome of cooperation, and the level of conflict may define the point at which cooperation is no longer a beneficial strategy for individuals. This possibility, that conflict at both inter-and intragroup levels define the stability of cooperation over time, remains relatively under-explored despite its potential importance in understanding the evolution of cooperation.
... The fact that gull embryos responded to adult alarm calls is in agreement with recent data showing the capacity of bird embryos to perceive parental calls that are used in different contexts 44,45 . However, the most important finding of our study is that unmanipulated embryos showed almost identical epigenetic and hormonal profiles and developed similar behaviours to those of their alarm-call-exposed clutch mates. ...
Article
Full-text available
During development in fluctuating environments, phenotypes can be adjusted to the conditions that individuals will probably encounter later in life. As developing embryos have a limited capacity to fully capture environmental information, theory predicts that they should integrate relevant information from all reliable sources, including the social environment. In many oviparous species, embryos are able to perceive cues of predator presence in some circumstances, but whether this information is socially transmitted among clutch mates—promoting phenotypic adjustments in the whole clutch—is unknown. Here, using an experimental design for which we modified the exposure to some, but not all, embryos of the same clutch to cues of predator presence (that is, alarm calls), we show that exposed embryos of the yellow-legged gull (Larus michahellis) and their unexposed clutch mates showed similar developmental changes that were absent in embryos from control clutches. Compared with the control broods, both embryos that were exposed to alarm calls and their unexposed clutch mates showed altered prenatal and postnatal behaviours, higher levels of DNA methylation and stress hormones, and reduced growth and numbers of mitochondria (which may be indicative of the capacity for energy production of cells). These results strongly suggest that gull embryos are able to acquire relevant environmental information from their siblings. Together, our results highlight the importance of socially acquired information during the prenatal stage as a non-genetic mechanism promoting developmental plasticity.
Article
Full-text available
En las especies con múltiples reproducciones, la inversión en reproducción a menudo disminuye el mantenimiento somático y la supervivencia, generando así un compromiso entre la reproducción actual y las oportunidades para reproducirse en el futuro. En esta pequeña reseña de nuestros estudios mostramos cómo este compromiso modula los conflictos de familia y las estrategias de inversión parental a lo largo de la vida, y puede ser determinado por las presiones de selección durante el desarrollo. Estudiamos cómo las señales sociales, incluidas las sexuales, afectan a las decisiones de inversión parental y pueden ser usadas por todos los miembros de la familia para ajustar su comportamiento, lo que provoca una coevolución social compleja. Nuestros estudios de seguimiento a largo plazo señalan que las estrategias de inversión cambian a lo largo de la vida y están afectadas por el valor de la presente reproducción y por las expectativas futuras. Diversos estudios indican que las trayectorias vitales pueden depender de las presiones selectivas a edades muy tempranas sobre un conjunto de rasgos, y el ambiente social puede ser determinante en su desarrollo. En las últimas décadas, el estudio de los rasgos de comportamiento ha ido cambiado; de examinar cada rasgo de forma independiente a estudiar las relaciones complejas entre rasgos o la coevolución con los rasgos de otros individuos en el entorno social. Quedan muchas preguntas por abordar y para resolverlas se necesitan nuevos estudios y modelos teóricos que recojan la complejidad de factores que afectan a los rasgos de comportamiento.
Article
Full-text available
Parents allocate resources to offspring to increase their survival and to maximize their own fitness, while this investment implies costs to their condition and future reproduction. Parents are hence expected to optimally allocate their resources. They should invest equally in all their offspring under good conditions, but when parental capacity is limited, parents should invest in the offspring with the highest probability of survival. Such parental favouritism is facilitated by the fact that offspring have evolved condition-dependent traits to signal their quality to parents. In this study we explore whether the parental response to an offspring quality signal depends on the intrinsic capacity of the parents, here the female. We first manipulated the intrinsic capacity of blue tit ( Cyanistes caeruleus ) females through lutein-supplementation during egg laying, and we subsequently blocked the UV/yellow reflectance of breast feathers on half of the nestlings in each brood. We did not find evidence that the female intrinsic capacity shaped parental feeding or sibling competition according to offspring UV/yellow colouration. However, nestling UV/yellow colour affected costly behavioural interactions in the form of prey-testings (when a parent places a prey item into a nestling’s gape but removes it again). In lutein-supplemented nests, fathers but not mothers favoured UV-blocked chicks by testing them less often, supporting previous results. Accordingly, in lutein-supplemented nests, UV-blocked nestlings gained more mass than their siblings, while in control nests we found the opposite effect and UV-blocked nestlings gained less. Our results emphasize that the prenatal environment shaped the role of offspring UV/yellow colour during certain family interactions and are indicative for sex-specific parental care strategies.
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1. Communication among family members is often essential for navigating the social and trophic interactions that arise during parental care. In insects, this communication is often accomplished via pheromonal signals. However, some insects also produce acoustic signals (stridulations) during parental care. 2. Burying beetles (Nicrophorus spp) audibly stridulate during mating and parental care and several studies have suggested that stridulation is an important form of communication between family members. Experimental studies have generally supported a role of stridulation in Nicrophorus parental care: preventing stridulation or changing the vibrational properties of stridulation generally reduces parental performance. However, some of these previous experiments are difficult to interpret and the importance of this form of communication in burying beetles is still unclear. 3. Here we describe experiments involving two Nicrophorus species (N. vespilloides and N. orbicollis) in which we used a minimally invasive phenotypic manipulation to test whether stridulation is necessary for effective parental care. Our phenotypic manipulation rendered the both species silent; however, it had no detectable impact on parental performance in either species. 4. Our results suggest that stridulation does not play an important role in mating or the coordination of parental care in at least two Nicrophorus species, casting doubt upon a long-assumed function of stridulation in the genus.
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In species where parents repeatedly provide their offspring with food, the offspring often communicate their need to the parents. Burying beetles, which breed on a wide size range of carcasses of small vertebrates, are interesting model systems to test theories on begging, because the larvae show partial begging, that is, they obtain food through both signalling to their parents (begging) and feeding directly from the carcass. We manipulated resource availability in Nicrophorus vespilloides by providing parents with mouse carcasses spanning a wide size range, and allowing them to rear the larvae that hatched, so that both the amount of resources and the number of siblings varied. Time spent begging by each larva was strongly influenced by the time parents spent near the larvae. Brood size had a nonlinear effect on larval begging, with begging increasing with brood size for relatively smaller broods and decreasing again for larger broods. Carcass size and number of parents present had no effect on begging. Time spent provisioning the larvae by the parents was strongly associated with the time spent begging by each larva. Parents spent more time provisioning under biparental care than under uniparental care, while brood size and carcass size had no significant effect. These findings suggest that the larvae adjust their begging to the behaviour of their parents and the number of siblings, but not to the amount of resources. Furthermore, parents adjust the time spent provisioning to the average amount of begging by each larva in the brood, and not to the availability of resources.
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Overt soliciting for parental resources, primarily food, is often explained as having evolved to express the fitness gain a signaling offspring would derive from a favorable parental response. This Signal of Need model makes 4 unheralded assumptions: 1) that parents' life-history objective is egalitarian; 2) that contemporaneous siblings participate nepotistically; 3) that dependent young can assess their own reproductive value from internal sources; and 4) that the morphological and behavioral signals we call "begging" are essential for transferring such cryptic information reliably. We review 2 parsimonious alternative types of honest begging. First, if the life-history assumption is relaxed, solicitation signals may be positively correlated with reproductive value, obviating the nepotism assumption. According to this Signal of Quality logic, solicitation signals can be seen as typical handicap-type advertisements of personal merit. Second, by relaxing the assumptions concerning cryptic fitness information entirely, solicitation signals might be purely proximate Signals of Hunger, with parents basing their overriding life-history decisions on nonsignal information streams (ecological costs of foraging plus offspring cues already in the public domain). These 3 hypotheses are easily testable, along with existing models that do not require parents to have complete control over resources. Copyright 2011, Oxford University Press.
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Interacting phenotypes are traits whose expression is affected by interactions with conspecifics. Commonly-studied interacting phenotypes include aggression, courtship, and communication. More extreme examples of interacting phenotypes-traits that exist exclusively as a product of interactions-include social dominance, intraspecific competitive ability, and mating systems. We adopt a quantitative genetic approach to assess genetic influences on interacting phenotypes. We partition genetic and environmental effects so that traits in conspecifics that influence the expression of interacting phenotypes are a component of the environment. When the trait having the effect is heritable, the environmental influence arising from the interaction has a genetic basis and can be incorporated as an indirect genetic effect. However, because it has a genetic basis, this environmental component can evolve. Therefore, to consider the evolution of interacting phenotypes we simultaneously consider changes in the direct genetic contributions to a trait (as a standard quantitative genetic approach would evaluate) as well as changes in the environmental (indirect genetic) contribution to the phenotype. We then explore the ramifications of this model of inheritance on the evolution of interacting phenotypes. The relative rate of evolution in interacting phenotypes can be quite different from that predicted by a standard quantitative genetic analysis. Phenotypic evolution is greatly enhanced or inhibited depending on the nature of the direct and indirect genetic effects. Further, unlike most models of phenotypic evolution, a lack of variation in direct genetic effects does not preclude evolution if there is genetic variance in the indirect genetic contributions. The available empirical evidence regarding the evolution of behavior expressed in interactions, although limited, supports the predictions of our model.
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Parents often have important influences on their offspring's traits and/or fitness (i.e., maternal or paternal effects). When offspring fitness is determined by the joint influences of offspring and parental traits, selection may favor particular combinations that generate high offspring fitness. We show that this epistasis for fitness between the parental and offspring genotypes can result in the evolution of their joint distribution, generating genetic correlations between the parental and offspring characters. This phenomenon can be viewed as a coadaptive process in which offspring genotypes evolve to function with the parentally provided environment and, in turn, the genes for this environment become associated with specific offspring genes adapted to it. To illustrate this point, we present two scenarios in which selection on offspring alone alters the correlation between a maternal and an offspring character. We use a quantitative genetic maternal effect model combined with a simple quadratic model of fitness to examine changes in the linkage disequilibrium between the maternal and offspring genotypes. In the first scenario, stabilizing selection on a maternally affected offspring character results in a genetic correlation that is opposite in sign to the maternal effect. In the second scenario, directional selection on an offspring trait that shows a nonadditive maternal effect can result in selection for positive covariances between the traits. This form of selection also results in increased genetic variation in maternal and offspring characters, and may, in the extreme case, promote host-race formation or speciation. This model provides a possible evolutionary explanation for the ubiquity of large genetic correlations between maternal and offspring traits, and suggests that this pattern of coinheritance may reflect functional relationships between these characters (i.e., functional integration).
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Evolutionary game theory1, ² is concerned with the evolutionarily stable outcomes of the process of natural selection. The theory is especially relevant when the fitness of an organism depends on the behaviour of other members of its population. Here we focus on the interaction between two organisms that have a conflict of interest. The standard approach to such two-player games is to assume that each player chooses a single action and that the evolutionarily stable action of each player is the best given the action of its opponent. We argue that, instead, most two-player games should be modelled as involving a series of interactions in which opponents negotiate the final outcome. Thus we should be concerned with evolutionarily stable negotiation rules rather than evolutionarily stable actions. The evolutionarily stable negotiation rule of each player is the best rule given the rule of its opponent. As we show, the action chosen as a result of the negotiation is not the best action given the action of the opponent. This conclusion necessitates a fundamental change in the way that evolutionary games are modelled.
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Introduction, In many bird species, young beg for care from their parents. A parent arriving at the nest with food is met by begging nestlings, which are waving their wings, calling and stretching to expose brightly coloured gapes, all within the confines of a nest that may contain several other begging nestlings. This mode of parent–offspring communication has become a model for the study of the evolution of biological signalling. Hungrier nestlings beg more intensely, so the parent can use the display to decide which nestling to feed and to decide how soon it should return to the nest with food (reviewed by Budden & Wright, 2001). The fact that the parent can extract information on nestling hunger from such a confusing burst of signalling raises numerous questions. How does each nestling ensure that its own signal of need is received above the din of its nestmates' displays? How do parents differentiate among these displays to choose which nestling to feed? How much do the displays, as opposed to the physical jostling toward the parent that also goes on in the nest, determine which nestlings are fed? To answer such questions we need to understand how the begging behaviours of whole broods function together. Concepts derived from the new field of communication networks seem well suited to this task but have not yet been explicitly applied to begging. As currently defined (McGregor & Dabelsteen, 1996; McGregor & Peake, 2000), a communication network forms whenever several individuals communicate within transmission range of each other's signals.
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Parents often have important influences on their offspring's traits and/or fitness (i.e., maternal or paternal effects). When offspring fitness is determined by the joint influences of offspring and parental traits, selection may favor particular combinations that generate high offspring fitness. We show that this epistasis for fitness between the parental and offspring genotypes can result in the evolution of their joint distribution, generating genetic correlations between the parental and offspring characters. This phenomenon can be viewed as a coadaptive process in which offspring genotypes evolve to function with the parentally provided environment and, in turn, the genes for this environment become associated with specific offspring genes adapted to it. To illustrate this point, we present two scenarios in which selection on offspring alone alters the correlation between a maternal and an offspring character. We use a quantitative genetic maternal effect model combined with a simple quadratic model of fitness to examine changes in the linkage disequilibrium between the maternal and offspring genotypes. In the first scenario, stabilizing selection on a maternally affected offspring character results in a genetic correlation that is opposite in sign to the maternal effect. In the second scenario, directional selection on an offspring trait that shows a nonadditive maternal effect can result in selection for positive covariances between the traits. This form of selection also results in increased genetic variation in maternal and offspring characters, and may, in the extreme case, promote host-race formation or speciation. This model provides a possible evolutionary explanation for the ubiquity of large genetic correlations between maternal and offspring traits, and suggests that this pattern of coinheritance may reflect functional relationships between these characters (i.e., functional integration).
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Interacting phenotypes are traits whose expression is affected by interactions with conspecifics. Commonly-studied interacting phenotypes include aggression, courtship, and communication. More extreme examples of interacting phenotypes-traits that exist exclusively as a product of interactions-include social dominance, intraspecific competitive ability, and mating systems. We adopt a quantitative genetic approach to assess genetic influences on interacting phenotypes. We partition genetic and environmental effects so that traits in conspecifics that influence the expression of interacting phenotypes are a component of the environment. When the trait having the effect is heritable, the environmental influence arising from the interaction has a genetic basis and can be incorporated as an indirect genetic effect. However, because it has a genetic basis, this environmental component can evolve. Therefore, to consider the evolution of interacting phenotypes we simultaneously consider changes in the direct genetic contributions to a trait (as a standard quantitative genetic approach would evaluate) as well as changes in the environmental (indirect genetic) contribution to the phenotype. We then explore the ramifications of this model of inheritance on the evolution of interacting phenotypes. The relative rate of evolution in interacting phenotypes can be quite different from that predicted by a standard quantitative genetic analysis. Phenotypic evolution is greatly enhanced or inhibited depending on the nature of the direct and indirect genetic effects. Further, unlike most models of phenotypic evolution, a lack of variation in direct genetic effects does not preclude evolution if there is genetic variance in the indirect genetic contributions. The available empirical evidence regarding the evolution of behavior expressed in interactions, although limited, supports the predictions of our model.
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Young CS1 mice aged 2, 4, 6, 8 and 10 days were each sequentially exposed to odours of urine from strange adult infanticidal and non-infanticidal males and the number of ultrasonic vocalizations monitored. There was a clear age effect, with pups 6–8 days calling the most. For pups of 2 and 6 days of age there were significant positive correlations between body weight and number of calls but for 10-day-old pups a negative correlation was found. Female pups called more than males, particularly when exposed to odours but this was not due to body weight. Overall, more calls were produced when odours from infanticidal rather than non-infanticidal males were presented and individual pups altered their ultrasonic output as the odours were changed.