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Kin selection theory predicts that cooperation is facilitated between genetic relatives, as by cooperating with kin an individual might increase its inclusive fitness. Although numerous theoretical papers confirm Hamilton's inclusive fitness theory, experimental evidence is still underrepresented, in particular in non-cooperative breeders. Cooperative predator inspection is one of the most intriguing anti-predator strategies as it implies high costs on inspectors. During an inspection event, one or more individuals leave the safety of a group and approach a potential predator in order to gather information about the current predation risk. We investigated the effect of genetic relatedness on cooperative predator inspection in juveniles of the cichlid fish Pelvicachromis taeniatus, a species in which juveniles live in shoals under natural conditions. We show that relatedness significantly influenced predator inspection behaviour with kin dyads being significantly more cooperative. Thus, our results indicate a higher disposition for cooperative anti-predator behaviour among kin as predicted by kin selection theory. This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.
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Kinship reinforces cooperative predator inspection in a
cichlid fish
UN K E N * §
*Institute for Evolutionary Biology and Ecology, University of Bonn, Bonn, Germany
Department of Fish Ecology and Evolution, Eawag Centre of Ecology, Evolution and Biogeochemistry, Kastanienbaum, Switzerland
Department of Aquatic Ecology, Eawag Centre of Ecology, Evolution and Biogeochemistry, Kastanienbaum, Switzerland
§Department of Behavioural Ecology, Institute for Ecology and Evolution, University of Bern, Hinterkappelen, Switzerland
inclusive fitness;
kin recognition;
kin selection;
tit for tat.
Kin selection theory predicts that cooperation is facilitated between genetic
relatives, as by cooperating with kin an individual might increase its inclu-
sive fitness. Although numerous theoretical papers support Hamilton’s
inclusive fitness theory, experimental evidence is still underrepresented, in
particular in noncooperative breeders. Cooperative predator inspection is
one of the most intriguing antipredator strategies, as it implies high costs on
inspectors. During an inspection event, one or more individuals leave the
safety of a group and approach a potential predator to gather information
about the current predation risk. We investigated the effect of genetic relat-
edness on cooperative predator inspection in juveniles of the cichlid fish
Pelvicachromis taeniatus, a species in which juveniles live in shoals under nat-
ural conditions. We show that relatedness significantly influenced predator
inspection behaviour with kin dyads being significantly more cooperative.
Thus, our results indicate a higher disposition for cooperative antipredator
behaviour among kin as predicted by kin selection theory.
The ubiquitous occurrence of cooperation (i.e. acts that
benefit others on own costs) among animals was
already extensively described by Darwin’s contempo-
raries (Kropotkin, 1902), and at that time considered as
potential problem for Darwin’s theory of natural selec-
tion (Darwin, 1859). Today, examples for cooperation
range from bacteria and microbes (e.g. Diggle et al.,
2007; L
opez-Villavicencio et al., 2011; Rumbaugh et al.,
2012; Inglis et al., 2014; Pollitt et al., 2014) to social
insects (Foster et al., 2005; Tibbets & Injaian, 2013) and
vertebrates (e.g. birds: Clutton-Brock, 2002; mammals:
Eberle & Kappeler, 2006; Dechmann et al., 2010; fish:
Taborsky, 1984). Some cooperative interactions can be
explained by an increase in direct fitness, for instance
because cooperation provides mutual benefits to both
actor and recipient (West et al., 2007), or because it is
based on reciprocal cooperation (Trivers, 1971; Schnee-
berger et al., 2012). However, a major step towards a
better understanding of social behaviour in general,
and cooperation in particular, was provided by Hamil-
ton’s (1964) inclusive fitness theory, stating that indi-
viduals do not maximize direct fitness but their
inclusive fitness, which can be indirectly achieved by
increasing the fitness of genetic relatives (Bourke,
2011). This theory allows explaining extreme forms of
altruism, which have, for example, evolved in eusocial
insects, where individuals forsake their own reproduc-
tion to raise their queen’s offspring (Hughes et al.,
2008), but it is also applicable to any other form of
social interaction (West & Gardner, 2010). Cooperative
strategies like reciprocity may be prone to cheating
(Kokko et al., 2001; Bergm
uller et al., 2010; Jiricny
et al., 2010), and thus, genetic relatedness between
interacting individuals may further facilitate the
evolution of cooperation.
Correspondence: Saskia Hesse, Institute for Evolutionary Biology and
Ecology, University of Bonn, An der Immenburg 1, D-53121 Bonn,
Germany. Tel.: +49 228 735749; fax: +49 228 732321; e-mail:
Data Archival Location: Attached to this file as supplementary
doi: 10.1111/jeb.12736
On the occasion of the 50th anniversary of Hamil-
ton’s and Maynard Smith’s papers (1963, 1964),
numerous reviews and theoretical papers stress the
importance of inclusive fitness theory (e.g. Van Dyken
& Wade, 2012; Lehmann & Rousset, 2014; McGlothlin
et al., 2014; Taylor & Maciejewski, 2014; Van Cleve &
ßay, 2014; Wild & Koykka, 2014). However,
although results of numerous correlative studies on
cooperation are in accordance with the predictions of
kin selection theory (Pfennig & Collins, 1993; H
et al., 1999; Gerlach et al., 2007; Markman et al., 2009;
Ruch et al., 2009; Chaine et al., 2010; Dobler & Koel-
liker, 2010), studies employing an experimental
approach are still underrepresented (but see Schneider
& Bilde, 2008; West et al., 2008; Rumbaugh et al., 2012;
Ho et al., 2013; Carazo et al., 2014; Hatchwell et al.,
2014). Most empirical studies address kin selection in
terms of cooperative breeding, which has been studied
in various vertebrate species (Clutton-Brock, 2002). For
example, kin selected benefits explain the evolution of
cooperation in birds (Komdeur, 1994; Russell & Hatch-
well, 2001; Hatchwell, 2009; Wright et al., 2010), and
mammals (Lukas & Clutton-Brock, 2012). Nevertheless,
even in cooperative breeders, inclusive fitness benefits
could be overestimated (Clutton-Brock, 2002), with
alternative explanations being possible (e.g. Kokko
et al., 2001; Clutton-Brock, 2009). For example, kinship
is often correlated with familiarity, which may con-
found effects of relatedness when it is not controlled
for (e.g. Penn & Frommen, 2010). In addition, nowa-
days there is convincing evidence that the evolution
and maintenance of cooperative breeding can be inde-
pendent from genetic relatedness among actors, and
that it can be driven by direct fitness benefits among
nonrelatives (Balshine-Earn et al., 1998; Queller et al.,
2000; Stiver et al., 2005; Riehl, 2010).
In the present study, we examine kin-biased coopera-
tion in a noncooperatively breeding fish. Fishes are a
major group in the study of the evolution of group
living (Krause & Ruxton, 2002). Several studies demon-
strated kin-biased shoaling preferences (e.g. Ward &
Hart, 2003; Gerlach & Lysiak, 2006; Frommen et al.,
2007) or kin-structured populations (e.g. Gerlach et al.,
2001; Piyapong et al., 2011; but see Croft et al., 2012).
Still, the adaptive significance of kin structuring often
remains unclear. Kin selection has been suggested as an
evolutionary force promoting and maintaining shoaling
with related individuals (Smith, 1986; Alfieri & Dugat-
kin, 2006). Especially, predator inspection offers an
excellent opportunity to study kin-biased cooperative
behaviour, because it has clear benefits and costs. Kin
selection has been postulated as a means to maintain
cooperation in predator inspection visits (for a detailed
discussion, see Wilson & Dugatkin, 1997; Thomas et al.,
2008). During predator inspection, one or more individ-
uals leave the safety of a group and inspect a potential
predator (Milinski, 1987; Dugatkin, 1988). By doing so,
they gain, on the one hand, information about the cur-
rent predation risk; on the other hand, they face high
costs in terms of an increase in predation risk (Du-
gatkin, 1992; Milinski et al., 1997). Predator inspection
is often carried out in pairs or small groups (Pitcher
et al., 1986), which is thought of as being beneficial, as
companions dilute the risk when staying close enough
to the leader (Milinski et al., 1997). Inspecting in
groups has been shown to follow complex behavioural
rules (e.g. Dugatkin, 1988; Dugatkin & Alfieri, 1991;
Pitcher, 1992). Cooperative predator inspection has
been explained using different theoretical approaches,
including reciprocal cooperation, group selection or
indirect genetic effects (e.g. Milinski, 1987; Wilson &
Dugatkin, 1997; Bleakley & Brodie, 2009). Milinski
(1987), for example, suggested that three-spined stick-
lebacks (Gasterosteus aculeatus) play ‘tit for tat’ when
confronted with a predator. In contrast, Thomas et al.
(2008) found no evidence for ‘tit-for-tat’ behaviour in
guppies (Poecilia reticulata).
The aim of our study was to investigate to what
extent cooperative predator inspection is influenced by
relatedness and whether kin selection can maintain
cooperation between related individuals, which has
been postulated, but until now, seldom been tested
experimentally. Thus, we tested whether dyads of juve-
nile cichlid fish composed of either unfamiliar kin or
unfamiliar nonkin differed in their predator inspection
behaviour. Our study animal, Pelvicachromis taeniatus,is
a small biparental cichlid fish capable of recognizing
kin through phenotype matching (Th
unken et al.,
2007; Hesse et al., 2012; Th
unken et al., 2014). Juve-
niles form loose shoals in nature (Lamboj, 2006) and
under laboratory conditions, and kin forms denser
shoals than nonkin (Hesse & Th
unken, 2014). Further-
more, juveniles engage in predator inspection beha-
viour (Hesse et al., 2015). Thus, juvenile P. taeniatus are
a suitable model organism to study the potential for
kin selection acting on the evolution of cooperative
Materials and methods
Study animal
Pelvicachromis taeniatus is a small, cave-breeding cichlid
from Western Africa. Our study population originated
from the Moliwe River in Cameroon (Langen et al.,
2011). Pelvicachromis taeniatus forms monogamous
pairs, and males and females prefer close kin as breed-
ing partners (Th
unken et al., 2007, 2012). Pelvi-
cachromis taeniatus performs biparental brood care and
free-swimming fry are guarded by both parents for
several weeks (Th
unken et al., 2010). Hereafter, juve-
niles live in shoals until they reach sexual maturity
(Lamboj, 2006). When given the choice between a
shoal of related and unrelated individuals, juvenile
P. taeniatus prefer shoaling with their kin (Th
et al., 2015).
Breeding of experimental fish
All experimental fish were bred under standardized con-
ditions between April and October 2011 at the labora-
tory of the Institute of Evolutionary Biology and
Ecology of the University of Bonn. Breeding pairs of
unrelated P. taeniatus (F1 generation of wild-caught fish)
were individually introduced into a breeding tank
(length 9width 9height: 45 cm 940 cm 930 cm,
one breeding pair per tank), which was equipped with a
breeding cave, an aquarium heater, an internal filter,
gravel and java moss (Taxiphyllum barbieri). The water
temperature was kept at 24 1°C and the light: dark
regime was 12:12 h. They were fed daily with a mixture
of defrosted Chironomus larvae, Artemia and black mos-
quito larvae. Until spawning occurred, approx. 30% of
the water was exchanged weekly to increase spawning
probability. Breeding caves were checked for eggs daily.
Rearing conditions of experimental fish
After spawning, eggs of 15 breeding pairs were
removed from the parents and raised artificially in
small tanks (30 cm 920 cm 920 cm). To examine the
effect of relatedness on cooperation independent from
familiarity, sibling groups were split 14 1 days after
hatching into two subgroups of 10 to 15 fish. By doing
so, we created similar sized groups of unfamiliar kin.
Fish were split after 14 1 days as mortality rates at
early larval stages (i.e. egg and wriggler stage) are
unpredictable and vary greatly between clutches. Sib-
ling groups were split shortly after individuals reached
the free-swimming stage. Test fish spent only the egg
(approx. 2 days) and larval stage (approx. 12 days)
together. Trials took place at least 4 months after split-
ting the groups. It is highly unlikely that fish can indi-
vidually recognize other fish with whom they spent a
few days as larvae in a group consisting of more than
20 larvae months ago, and adjust their current beha-
viour based on those prior experiences and interactions
with them (see also Utne-Palm & Hart, 2000). Thus,
confounding effects based on familiarity are extremely
unlikely. Each sibling group was housed in a tank
(45 cm 940 cm 930 cm) equipped with sand, java
moss and an internal filter. All tanks were surrounded
by opaque plastic sheets to prevent visual contact
between inhabitants of different tanks. The water tem-
perature was kept at 23 1°C, and the experimental
subjects were held under a light: dark regime of
12:12 h. Free-swimming fry were first fed with living
Artemia nauplii provided in a standardized, highly con-
centrated suspension (10 ll per fish). Later on, fish
were fed daily in excess with a mixture of defrosted
Chironimus larvae, Artemia and black mosquito larvae.
We used five snakeheads (Parachanna obscura, mean
total length =13.25 SD 1.37 cm) as predators. P.
obscura is a sit-and-wait predator, which occurs in the
same habitat as P. taeniatus (Bonou & Teugels, 1985).
Snakeheads are an established predator model for the
study of antipredator behaviour (e.g. Kelley & Magur-
ran, 2003; Botham et al., 2006; Hesse et al., 2015). They
were obtained from a commercial fish trader (Pan-
taRhei Aquaristik, Wedemark) and housed individually
in tanks (45 cm 940 cm 930 cm) equipped with an
internal filter, gravel, plants (java moss (Taxiphyllum
barbieri), java fern (Microsorum pteropus)) and rocks to
provide shelter. The water temperature was kept at
23 1°C, and the light: dark regime was set to
12:12 h. Snakeheads were fed every 3 days with a
freshly killed P. taeniatus.
Experimental set-up
The experimental tank (70 cm 935 cm 935 cm,
water level 12 cm) was divided into three compart-
ments: a predator compartment (15 cm), an experi-
mental compartment (38.5 cm) and an acclimatization
compartment containing a plastic plant as refuge
(16.5 cm) (Fig. 1) (cf. Frommen et al., 2009). The
acclimatization compartment was separated from the
rest of the tank by a removable, opaque plastic partition
to ensure an undisturbed acclimatization period. A
transparent perforated plastic partition (permitting
visual as well as olfactory contact between prey and
predator) separated the predator compartment from the
experimental compartment. The experimental compart-
ment contained an inspection zone (22 cm) directly in
front of the predator compartment. The size of the
inspection zone was based on the size of the predators
and the highest predation risk found in the literature
based on fast start performance of teleost fish (Webb,
1978; Domenici & Blake, 1997) and on an experiment
on risk allocation (Milinski et al., 1997). Pretests
revealed that the behaviour in the inspection zone was
different from normal shoaling behaviour. Within this
distance to the predator, fish showed inspection beha-
viour, that is they approached the predator purpose-
fully, stopped near the predator and then slowly
departed it again (Pitcher et al., 1986). All compart-
ments were marked on the bottom by black lines.
To avoid interactions of test fish with their reflec-
tions, the experimental tank was covered with grey
plastic sheets on the inner sides. Additionally, the
experimental tank was surrounded with white Styro-
foam to minimize disturbance. The tank was filled with
aged, substrate-treated tap water (23 1°C) (for a
detailed explanation, see Meuthen et al., 2011) to a
height of 12 cm. After each experiment, it was cleaned,
rinsed with hot water and refilled. Behaviours of test
Kin-biased cooperation in predator inspection 3
fish were recorded by a webcam (Logitech Webcam,
Pro 9000) attached to a wooden frame placed 70 cm
above the centre of the tank. The experimental tank
was illuminated from above by a fluorescent tube
(Osram Lumilux L, 58W).
Experimental procedure
To investigate cooperative predator inspection, a pair of
unfamiliar juvenile fish differing in relatedness was
tested (full-sibling pairs vs. nonkin pairs). Fish were
carefully netted and each was placed in a small plastic
tank (17 cm 910 cm 910 cm, water level 5 cm).
Characteristic fin patterns (dots) were recorded to
recognize individual test fish, so fish could be placed
back into their corresponding home tanks after the
experiment. Test fish were immature, so their sex could
not be determined definitely. Each fish was only tested
A snakehead was carefully netted and introduced
into the predator compartment. No predator was used
more than twice each day. Test fish were then trans-
ferred into the experimental tank by gently and simul-
taneously pouring them from the plastic tanks into the
acclimatization compartment. They were allowed to
acclimatize for 45 min. Subsequently, the opaque parti-
tion separating the acclimatization compartment from
the experimental compartment was lifted using a pulley
system. As our experimental fish were predator na
individuals, we used a conspecific alarm cue (1 ml) that
was added at the centre of the tank just before the trial
started to elicit a stronger antipredator response, to
increase the vigilance of test fish and stimulate the
predator (Alemadi & Wisenden, 2002; Ferrari et al.,
2009). Individuals used for alarm cue extraction were
unrelated adult fish and the whole fish was used (for
further details, see Meuthen et al., 2014). Each experi-
ment lasted 45 min. Afterwards, the standard body
length (SL =distance from the tip of the snout to the
beginning of the caudal fin) of the test fish was mea-
sured. There was no significant size difference between
fish of the two treatment groups (linear mixed-effects
model (LME), LRT: v
=1.739, d.f. =1, P=0.187, mean
difference in SL
unfamiliar kin
SD =0.51 0.41 cm,
mean difference in SL
unfamiliar nonkin
SD =0.39
0.2 cm).
Data acquisition
Videos were examined naively with regard to the iden-
tity of the test fish. After one fish entered the inspec-
tion zone, the trial started and the consecutive 400s
were analysed. We chose this time frame since test fish
habituated to the presence of predators with elapsed
time (S. Hesse, personal observation). Snapshots were
taken of each video every 5 s, that is 80 snapshots/trial.
If both focal fish had not entered the inspection zone
after 45 min, experiments were excluded from analysis
(N=5). We distinguish between two different types of
inspections behaviour: (1) cooperative inspections or
(2) solitary inspections. In a cooperative inspection,
both fish entered the inspection zone either simulta-
neously or time-delayed (i.e. the snapshot shows two
fish in the inspection zone) and a cooperative inspec-
tion ended when one fish left the inspection zone (i.e.
the snapshot of a previously cooperatively inspecting
dyad shows only one fish in the inspection zone). A
solitary inspection was defined as only one fish enter-
ing the inspection zone (i.e. snapshot showing only one
fish in the inspection zone) or a fish being abandoned
by its companion fish (thus remaining in the inspection
zone alone; only one fish present in the snapshot of a
previously cooperatively inspecting dyad) and number
of defections (number of events when one test fish was
abandoned during predator inspection for each pair) for
each trial was noted. A single inspection event ended
either when the inspector left the inspection zone, or
when the other fish entered the inspection zone (i.e.
Experimental compartment
Fig. 1 Experimental set-up viewed
from the side. The experimental tank
(70 cm 935 cm 935 cm) was divided
into three compartments: predator
compartment (15 cm), experimental
compartment (38.5 cm) containing the
inspection zone (22 cm) and an
acclimatization compartment (16.5 cm).
The predator compartment was
separated from the rest of the tank
through a transparent perforated plastic
sheet. The acclimatization compartment
containing a plastic plant as refuge was
separated by a removable opaque
plastic sheet.
time-delayed cooperative inspection). All inspection
events were measured per dyad and not per individual
fish as fish could not be individually distinguished from
the snapshots. We recorded the time fish spent inspect-
ing the predator either cooperatively or solitarily (time
(s) inferred by the 5-sec snapshots spent in either coop-
erative or solitary inspection). To analyse the data,
median values of each dyad were used.
Data analysis
In total, 46 valid trials were performed (unfamiliar kin:
N=21, unfamiliar nonkin: N=25). Analyses were
performed with the R. 2.9.1 statistical software package
R-Development-Core-Team (2009). Data were normally
distributed according to Lilliefors test and showed
homogeneous variances according to Bartlett tests so
linear mixed-effect models (LMEs) were run. Reported
P-values of models refer to the increase in deviance
when the respective variable was removed. Tests of sta-
tistical significance were based on likelihood ratio tests
(LRT), which follow a chi-square distribution. These
routines use maximum-likelihood parameter estima-
tion. Nonsignificant factors were removed from the
models. P-values are two-tailed throughout. Time spent
in cooperative inspections was the dependent variable,
kinship and body size difference were the explanatory
variables, and family combination was entered as ran-
dom factor and never removed to correct for multiple
use of families. Time spent in solitary inspections and
number of defections was also included as explanatory
variables to test whether they affected time spent in
cooperation. Additionally, the impact of relatedness on
the time spent in solitary inspections using family
means was examined using Wilcoxon rank sum test.
Family means were used to analyse time spent in soli-
tary inspection as data failed normal distribution after
transformation. Number of defections was also exam-
ined using Wilcoxon rank sum test. Family means were
used as data showed overdispersion.
Kinship explained differences in time test fish spent in
cooperative inspections (LME, LRT: v
d.f. =1, P=0.001, Fig. 2). Time spent in cooperative
inspections was negatively related to time spent in soli-
tary inspection (LME, LRT: v
=15.305, d.f. =1,
P<0.001), whereas body size difference (LME, LRT:
=1.783, d.f. =1, P=0.182) and number of defec-
tions (LME, LRT: v
=0.305, d.f. =1, P=0.861) did
not significantly explain variation in time spent in
cooperative inspections. Dyads consisting of nonkin
spent significantly more time involved in solitary
inspections events compared to dyads consisting of
unfamiliar kin (mean
SD =40.385s 61.134,
SD =112.115s 103.237; Wilcoxon rank
sum test, W=33.500, P=0.001, Fig. 3). Number of
defections did not differ significantly between kin and
nonkin (mean
SD =0.885 0.860, mean
SD =1.192 1.182; Wilcoxon rank sum test,
W=72.5, P=0.542).
Predation is among the strongest selective forces affect-
ing the fitness of an individual (Lima & Dill, 1990). By
inspecting a potential predator, valuable information
may be gained upon the identity of the predator, its
hunger status and intentions (Dugatkin, 1992). Cooper-
ative predator inspection is a strategy to deal with pre-
dation. Here, we investigated differences in cooperative
predator inspection behaviour between kin and nonkin
dyads to evaluate the influence of kinship on this dan-
gerous behaviour. Dyads of related P. taeniatus were sig-
nificantly more often involved in cooperative predator
inspections than nonkin dyads. The time test fish spent
in solitary inspections also significantly explained the
time test fish spent in cooperative inspection, indicating
that cooperating individuals spent less time inspecting
alone. Nonkin dyads performed significantly more soli-
tary inspections, indicating a lower disposition to coop-
erate compared to kin dyads. In accordance with the
predictions of kin selection theory (Hamilton, 1964),
the results of the present study reveal that kinship
enforces cooperation, in our case cooperative predator
inspections in a fish.
Inspecting a predator also provides valuable direct fit-
ness benefits for inspecting fish (Dugatkin & Godin,
1992; Pitcher, 1992) and explains why test fish engaged
frequently in this highly risky behaviour alone. Direct
information on type and hunger status of the predator
allows prey to adjust their behaviour to the current
predation threat, for example whether to stop foraging.
However, a study performed with guppies by Dugatkin
(1992) demonstrated how dangerous inspection visits
Time (s) spent in cooperave inspecons
Kin Non kin
Fig. 2 Mean time SE (s) test fish spent in cooperative
inspections during the trial (total time: 400 s). ***Indicates
Kin-biased cooperation in predator inspection 5
are. In that study, the tendency to approach a predator
predicted mortality risk of individual guppies: fish
engaging frequently in predator inspections were more
likely to die (Dugatkin, 1992). Therefore, a cooperative
predator inspection strategy like ‘tit for tat’ relying on
frequent interactions between cooperating individuals is
less beneficial if mortality risk is high, thus resulting in
the death of one (or more) familiar players. In such a
high-risk scenario, kin selection may facilitate coopera-
tion between relatives and provide direct as well as
indirect fitness benefits for inspectors and noninspectors
(i.e. the rest of the shoal as information is transmitted,
e.g Dugatkin & Godin, 1992). In shoals, small fish and
especially juveniles are highly exposed to predation, as
small prey is preferred by predators (see Sogard, 1997
for a review). If kin is more willing to cooperate,
reciprocation between familiar individuals is no longer
a prerequisite for cooperative predator inspection,
especially if shoals (or populations) are kin-structured.
Consequently, our results suggest that apart from
cooperation triggered by reciprocal altruism, kin
selection facilitates cooperation among unfamiliar
Besides kin selection, cooperation during predator
inspection may be maintained by several mechanisms
including by-product mutualism (Connor, 1995, Ste-
phens et al., 1997) and reciprocity (Milinski, 1987). The
number of defections did not negatively affect the
degree of cooperative behaviour (i.e. time spent in
cooperative inspections). A negative correlation
between number of defections and cooperation would
be expected especially in a ‘tit-for-tat’-like scenario.
Our result is consistent with a study performed in gup-
pies, showing that defection during predator inspection
did not affect subsequent cooperative behaviour of
defected individuals (Thomas et al., 2008).
Several laboratory studies showed kin shoaling pref-
erences in fishes, including cichlids (e.g. reviewed in
Ward & Hart, 2003; Frommen et al., 2007; Lee-Jenkins
& Godin, 2013). Still, the adaptive significance is often
ambigous. Benefits of grouping with kin are suggested
to include improved responses to predators (Hain &
Neff, 2009) and increased shoal cohesion (Hesse &
unken, 2014), increased growth rates (Gerlach et al.,
2007; Th
unken et al., 2015) and less aggression (Olsen
et al., 1996). Still, other studies did not describe such
advantages (e.g. Mehlis et al., 2009). Interestingly,
Piyapong et al. (2011) found kin aggregation only in
predator rich habitats, pointing towards a link between
predatory environment and kin-triggered social aggre-
gations. In our study, we provide evidence how kin
recognition leads to kin-directed antipredator benefits
in such a risky environment.
In summary, our results indicate that kinship influ-
ences and shapes cooperative behaviour in a predation
context. As predicted by kin selection theory, risk shar-
ing and cooperation was kin-biased; related dyads of
juvenile P. taeniatus were more willing to cooperate.
Although predator inspection scenarios have tradition-
ally been used to investigate the evolution of coopera-
tion based on reciprocity, our experiment demonstrates
for the first time that cooperation during predator
inspection may also be based on kinship. Therefore, our
study increases our understanding of how kin-directed
benefits facilitate the evolution of cooperation.
Ethical statement
The experiments comply with the current laws in the
country in which they were performed.
Conflict of interest
The authors declare that they have no conflict of
This work was supported by a grant of the Deutsche
Forschungsgemeinschaft (TH 1516/1-1).
We would like to thank Theo C.M. Bakker for logistical
support. The manuscript greatly benefitted from
thoughtful comments of two anonymous referees.
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Time spent in single inspecons (%)
Kin Non kin
Fig. 3 Mean time (% of 400s trials) test fish spent in solitary
inspections during the trial. Whiskers indicate standard error,
**Indicates P<0.01.
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Supporting information
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online version of this article:
Data S1 Supporting information.
Received 24 February 2015; revised 17 June 2015; accepted 28 July
Kin-biased cooperation in predator inspection 9
... Breeding pairs are socially monogamous and exhibit biparental brood care, which is performed more vigorously if the parents are related to each other (Thünken et al., 2007a). A few weeks after hatching, juveniles leave their parents and form loose shoals, which are more cohesive (Hesse & Thünken, 2014) and more cooperative during predator inspection (Hesse et al., 2015), when the shoal consists of kin. In contrast, there is evidence for kin avoidance and aggressiveness during intrasexual competition. ...
... Still, despite being able to recognize kin, female P. taeniatus did not conform to this pattern. Therefore, it is likely that kin cooperation in P. taeniatus is a phenomenon among juveniles, for instance expressed by greater cooperation during predator inspection (Hesse et al., 2015), and mating partners, decreasing intersexual aggression and increasing guarding behaviour for young (Thünken et al., 2007a). At the onset of sexual maturity, dominant females may no longer differentiate between sisters and unrelated females and direct aggression against any potential same-sex competitor. ...
... Contrary to expectations, hierarchy steepness and food monopolization were not influenced by genetic relatedness, stressing the context dependence of kin selection. In the same species, kinbiased cooperation among gregarious juveniles and monogamous breeding pairs (Hesse et al., 2015;Thünken et al., 2007a) is accompanied by intrasexual kin avoidance (Vitt, Madge Pimentel, Thünken, 2020) and increased aggression among brothers (Vitt, Hiller, Thünken, 2020), as well as indiscriminate despotism in females, as shown in the present study. Social hierarchies play an important role in food competition in cichlid fish and the benefits of dominance manifest under highly restricted feeding conditions by less severe losses in body mass for high-ranking females. ...
Kin selection theory predicts that genetic relatedness between group members can reduce the asymmetry in resource partitioning between superior and inferior competitors. In social groups, access to resources is often regulated by dominance hierarchies; thus, the degree of relatedness within a group may have a substantial impact on hierarchy structure. However, evidence of such effects is scarce. This study investigated how genetic relatedness and food competition affect dominance hierarchies in adult female Pelvicachromis taeniatus, a biparental African cichlid that shows kin-directed cooperation during juvenile shoaling and parental care. We compared triads of unfamiliar females, consisting of either a sister pair and an unrelated female (‘mixed’ groups) or three unrelated females (‘nonkin’ groups), and measured food monopolization and hierarchy characteristics (linearity, hierarchy steepness and short-term stability). To determine dominance relationships, we used an automated analysis of approach–avoidance events based on video-tracking data. The females formed hierarchies that remained stable over 2 days and were linear or near linear with one clear alpha female dominating the other two group members. Higher-ranking females tended to have prior access to food and could better sustain their body mass. The steepness of these hierarchies decreased after feeding, showing that dominance behaviour changed plastically depending on the intensity of competition over limited resources. Mixed groups consumed food slower than nonkin groups, but the treatments did not differ in food monopolization or hierarchy characteristics. In conclusion, kin-biased behaviour was highly dependent on life stage and social context: Within the same species, juveniles and mating partners showed increased cooperation, whereas female–female competition and dominance remained unaffected by genetic relatedness.
... This has also been confirmed for multiple fish species, for which social recognition and attraction can be mediated by sex [2], body size [3], shoal size [4], body coloration [5], health status (e.g., external indicators of parasitism [6]), behaviour [7], relatedness [8], and familiarity [9]. Associating with either kin (genetically related) or familiar (with sufficient amount of time of interaction and sharing of activities between the individuals) fishes has several benefits for individuals' fitness and survival, as it promotes growth [10], enhances cooperative behaviour [11], improves group antipredator behaviour [12], enhances foraging activity [13], reduces aggression between individuals within the group [14], and even promotes learning abilities [14][15][16]. ...
... In the control experiment, when both end compartments of the experimental tank were empty, sand smelt larvae spent approximately the same time on each preference zone (10.811 ± 2.077% vs. 14.811 ± 3.132%, Z (11) = 1.067, p = 0.286) and performed the same number of visits to each preference zone (22.035 ± 3.402% vs. 26.097 ± 3.289%, Z (11) ...
... When only chemical cues were available, sand smelt larvae spent little time close to natal reef fish (4.390 ± 2.535%) and non-natal reef fish (8.110 ± 3.870%) (Z (11) = 0.489, p = 0.625; see Tables 1 and 2, Figures 3A and 4A). The frequency of visits to natal and non-natal stimulus shoals averaged 13.060 ± 4.127% vs. 21.330 ...
Full-text available
The ability of shoaling fish to recognise and differentiate between potential groupmates may affect their fitness and survival. Fish are capable of social recognition and multiple sensory cues mediate the recognition mechanisms. This has been comprehensively studied for juvenile and adult freshwater species. However, the recognition ability and mechanisms intervening during the larval phase of marine species are yet poorly understood. Fish larvae are capable of discriminating conspecifics from heterospecifics based on chemical and/or visual cues, but whether this recognition occurs at finer scales, such as discerning among conspecifics of different reefs, is yet understudied. Here, we tested the hypothesis that larvae of a marine fish species, the sand smelt (Atherina presbyter Cuvier, 1829), are able to recognise and associate with conspecifics of their natal reef versus conspecifics of a non-natal reef based on three sensory modalities—chemical, visual, and chemical and visual simultaneously. Results do not support our hypothesis, but still provide evidence of group cohesion and indicate large differences in the relative importance of the different senses when associating with conspecifics, with visual cues playing a more important role than chemical cues alone.
... High levels of within-group relatedness can furthermore lead to higher survival due to optimized cooperative antipredator behavior. For (Josi, Taborsky, & Frommen, 2019 (Hesse, Anaya-Rojas, Frommen, & Thünken, 2015a). Finally, kin-biased cooperation in fishes might be important during reproduction. ...
... Furthermore, inspection may not always be done in pairs, but also by singletons or small groups (Pitcher, 1992), requiring extended explanations for such cooperative behavior, which need not to be mutually exclusive (Milinsk, Pfluger, Külling, & Kettler, 1990). For example, relatedness of group members has been shown to reinforce reciprocal predator inspection in P. taeniatus (Hesse et al., 2015a). ...
Cooperative interactions are widespread in the animal kingdom. Their occurrence can be explained by mutually non-exclusive benefits increasing an individual's (1) indirect fitness by cooperating with kin, and (2) direct fitness by mutually or reciprocally cooperating with others. Many cooperative behaviors require well-developed neuroendocrine mechanisms regulating their quantity and quality. Fishes offer great opportunities to increase our insight into ultimate and proximate questions of cooperation. Their social systems range from solitary- and pair-living to lose fission–fusion groups and highly complex societies. Cooperative interactions are an essential part of the behavioural repertoire of most fish species, occurring in a variety of social situations like predator inspection, foraging, mating, or brood care. Such interactions take place among related and unrelated individuals and even between members of different species. This fascinating diversity allows investigating all crucial factors mediating cooperation, e.g., by studying behavioural interactions within and between species, by applying comparative approaches between taxonomic groups and by using state-of-the-art genetic and neuroendocrine technologies to resolve the underlying mechanisms. This chapter provides an overview of the mechanisms and functions of cooperative behaviour in fishes, with the overall aim to illuminate the evolution of cooperative behaviour in general.
... Kin discrimination, that is, the differential treatment of kin and nonkin based on kin recognition (the cognitive ability to differentiate between related and unrelated individuals (Hepper, 2005;Mateo, 2004;Penn & Frommen, 2010)) is widespread in animals. Kin discrimination is relevant in diverse contexts ranging from mate choice (reviewed in Szulkin, Stopher, Pemberton, & Reid, 2013), grouping decisions to cooperation and aggression in groups (Brown & Brown, 1993a, 1993bEdenbrow & Croft, 2012;Griffiths & Armstrong, 2002;Hesse, Anaya-Rojas, Frommen, & Thünken, 2015;Makowicz, Moore, & Schlupp, 2018;Thünken, Hesse, Bakker, & Baldauf, 2015). Generally, kin discrimination in intrasexual selection has received less attention and, in particular, experimental evidence for higher aggression against related competitors is scarce. ...
Full-text available
During intrasexual competition, individuals of the same sex compete for access to breeding sites and mating partners, often accompanied by aggressive behavior. Kin selection theory predicts different kin‐directed social interactions ranging from cooperation to aggression depending on the context and the resource in question. Kin competition reducing indirect fitness might be avoided by actively expelling relatives from territories and by showing higher aggression against kin. The West‐African cichlid Pelvicachromis taeniatus is a monogamous cave breeder with males occupying and defending breeding sites against rivals. This species is capable of kin recognition and shows kin‐preference during juvenile shoaling and mate choice. However, subadults of P. taeniatus seem to avoid the proximity of same‐sex kin. In the present study, we examined territorial aggression of territory holders against intruding related and unrelated males as well as intruder's behavior. We observed higher aggression among related competitors suggesting that related males are less tolerated as neighbors. Avoidance of intrasexual competition with relatives might increase indirect fitness of males in monogamous species. Kinship promotes intrasexual aggression in a territorial context. Confronting male territory holders with related and unrelated intruders results in higher aggression when the intruders are related. Expulsion of related rivals may ultimately lead to reduced intrasexual kin competition over mating partners.
... Nevertheless predator inspection flights, i.e. approaching to gather some information and mobbing are not mutually exclusive. However, predator inspection behaviour is more common than mobbing (Pitcher et al. 1986;FitzGibbon 1994;Carter et al. 2015;Hesse et al. 2015). ...
Distress calls are known from a variety of animals and are defined as vocalisations emitted during extreme physical stress. Even though distress calls have been studied for a long time, their precise advantage for callers or the significance for receivers is still unclear. In this study, we describe distress calls of the nectarivorous bat Glossophaga soricina (Phyllostomidae: Glossophaginae). Analysing 1925 distress call syllables from 15 individuals caught in the field, we defined six different syllable types. Distress calls were high-intensity, broadband sounds with a low frequency range and thus comparable to those of other taxa. We found statistical evidence for an individual signature in distress calls, but not for a sex-specific signature. Further, playback experiments revealed that group-housed bats responded to distress calls, whereas single-housed bats did not, suggesting that the bats' response behaviour is influenced by group size. Bats responded significantly to normal and distorted conspecific distress calls but not to heterospecific distress calls. We found no sex-specific differences in the response to different playback stimuli. In conclusion, our results indicate that distress calls of bats encode important social information that can be used by receivers and that the response behaviour of receivers depends on the presence of conspecifics.
... For instance, female rainbowfish (Melanotaenia eachamensis) show significant association preferences for samesex siblings, but avoided their male siblings, suggesting that they are able to balance the benefits of kin association against the potential costs of inbreeding (Arnold, 2000). The benefits of associating with kin can range from faster growth rates to greater shoal cohesiveness and increased co-operation (Hain and Neff, 2009;Hesse and Thünken, 2014;Hesse et al., 2015;Thünken et al., 2015). ...
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Social aggregation is a widespread and important phenomenon among fishes. Understanding the questions of why and how aggregations form and are subsequently maintained is a central goal for behavioral ecologists. Research in this field has shown that aggregations are typically structured, non-random associations. This indicates that fish are able to differentiate between potential group-mates and that this ability mediates their association preferences, and, ultimately, the composition of their groups. In this review, we examine the characteristics that influence the expression of social attraction among fishes, before going on to describe the recognition mechanisms that underpin social attraction. Finally, we highlight a number of outstanding questions in the field with a view to generating a more complete understanding of social aggregation in fishes.
... Juveniles prefer to shoal with (familiar) kin, which appears to be adaptive because juveniles grow better in groups consisting of kin only (Thünken et al. 2016). Additionally, related individuals form tighter shoals (Hesse and Thünken 2014) and are more cooperative during predator inspection than unrelated conspecifics (Hesse et al. 2015). ...
Inclusive fitness theory predicts that individuals can increase their indirect fitness by grouping with kin. However, kin grouping also increases competition between kin, which potentially outweighs its benefits. The level of kin competition is contingent on environmental conditions and thus highly variable. Hence, individuals should benefit from plastically adjusting kin discrimination according to the expected level of kin competition. Here, we investigate whether perceived high competition affects juvenile kin-shoaling preferences in the cichlid Pelvicachromis taeniatus. Juveniles were given the choice between two shoals consisting of either kin or nonkin. Levels of perceived competition were manipulated through food limitation in the face of the differential energy expenditure of differently sized fish. The preference to shoal with kin decreased with increasing levels of perceived competition; small food-deprived individuals avoided kin. Shoaling with kin under strong competition may reduce individual indirect fitness. Hence, individuals can likely improve their inclusive fitness by plastically adjusting their kin-grouping preferences.
... For example, disturbance cues may reduce the predator's ability or willingness to attack (Smith, 1992), and this may be bolstered when shoalmates simultaneously produce disturbance cues. Fish are known to cooperate more in predator-deterring behaviours such as predator inspections when present alongside familiar shoalmates (Chivers et al., 1995;Hesse, Anaya-Rojas, Frommen, & Thünken, 2015). However, ...
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Animal signalling systems outside the realm of human perception remain largely understudied. These systems consist of four main components: a signalling context, a voluntary signal, receiver responses and resulting fitness benefits to both the signaller and receiver(s). It is often most difficult to determine incidental cues from voluntary signals. One example is chemical disturbance cues released by aquatic prey during predator encounters that may serve to alert conspecifics of nearby risk and initiate tighter shoaling. We aimed to test whether disturbance cues are released incidentally (i.e. as a cue) or are produced voluntarily depending on a specific signalling context such as the audience surrounding the individual, and thus constitute a signal. We hypothesized that if receivers use disturbance cues to communicate risk among themselves, they would produce more (or more potent) disturbance cues when present in a group of conspecifics rather than when they are isolated (presence/absence of an audience) and use disturbance cues more when present alongside familiar rather than unfamiliar conspecifics (audience composition effect). We placed fathead minnows (Pimephales promelas) in groups with familiar fish, unfamiliar fish or as isolated individuals with no audience present, and then simulated a predator chase to evoke disturbance cues. We used bioassays with independent receivers to assess whether the disturbance cues produced differed depending on the signallers’ audience. We found evidence of voluntary signalling, as minnows responded to disturbance cues from groups of fish with tighter shoaling while disturbance cues from isolated minnows did not evoke a significant shoaling response (presence/absence audience effect). Receivers also increased shoaling, freezing and dashing more in response to disturbance cues from familiar groups compared to disturbance cues from unfamiliar groups or isolated minnows (audience composition effect). Together, these findings support our hypothesis that disturbance cues are used as an antipredator signal to initiate coordinated group defences among familiar conspecifics involving shoaling, freezing and dashing. This study represents the strongest evidence to date that chemicals released by aquatic prey upon disturbance by predators serve as voluntary signals rather than simply cues that prey have evolved to detect when assessing their risk of predation. The authors found evidence of a novel chemical alarm signalling system in aquatic prey. Fathead minnows produced chemical disturbance cues more when present alongside an audience of familiar minnows compared to unfamiliar minnows or by themselves. Disturbance cues are thus signals targeted at specific audiences and used to coordinate group shoaling.
While the importance of kin discrimination, that is, kin recognition and subsequent differential treatment of kin and nonkin, is well established for kin-directed cooperation or altruism, the role of kin discrimination in the context of kin competition and kin avoidance is largely unexplored. Theory predicts that individuals avoiding competition with kin should be favored by natural selection due to indirect fitness benefits. Using an experimental approach, we investigated whether the presence of same-sex kin affects avoidance and explorative behavior in subadult Pelvicachromis taeniatus, a West African cichlid fish with strong intrasexual competition in both sexes. Pelvicachromis taeniatus is capable of recognizing kin using phenotype matching and shows kin discrimination in diverse contexts. When exposed to a same-sex conspecific, both males and females tended to interact less with the related opponent. Moreover, individuals explored a novel environment faster after exposure to kin than to nonkin. This effect was more pronounced in females. Individuals avoiding the proximity of same-sex relatives may reduce kin competition over resources such as mating partners or food.
Fish often undergo predation stress and food shortages in nature, and living in groups may provide the ecological benefits of decreased predator risk but the costs of increased food competition. The main aim of the present study was to test whether the behavioral response of qingbo (Spinibarbus sinensis) to predators and/or starvation differed between a singleton and a group. We measured the locomotor activity and distance to a predator and/or food item of prior predator-experienced, starved, double-treated and control qingbo; the qingbo were tested both as singletons and in a group (five individuals). Fish from all groups showed increased activity when tested collectively compared to individually. The predator-experienced fish showed decreased locomotor activity to predators as an antipredator strategy when tested as singletons; however, increased locomotor activity occurred when tested in a group, which might be partially due to the decreased predator risk when living in a group and thus higher levels of boldness. As expected, starvation elicited increased activity indicating increased foraging willingness when tested in a group; however, the difference between starved and normal-fed fish was no longer significant when they were tested as singletons, possibly due to the increased predation risk and decreased food competition when living individually and higher behavioral variation among individual fish than among those in a shoal. Compared with the control fish, the double-treated fish showed no difference in activity when tested both individually and collectively (except a slower speed when tested in a group). The reason for the results from the singletons might be an offset of the effect of predator exposure and starvation. The reason for this difference in the group might be due to the impaired body condition indicated by a slower swimming speed as a consequence of severe stress. The present study demonstrated that behavioral adjustment was closely related to the size of the group, which might be due to differences in the predation risk and food competition.
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Group living is widespread in animals. In nature, groups usually not only differ in phenotypic characteristics but also in the social relationships among group members. Theory predicts that individuals adjusting their shoaling decisions—to join certain groups or not—based on social criteria, such as familiarity or genetic relatedness, can increase their fitness. Although numerous studies report grouping preferences based on social criteria, the benefits actually emerging from such behavioral preferences are less well studied. Here, we examine both shoaling preferences and their consequences in juveniles of Pelvicachromis taeniatus, a monogamous cichlid fish from Western Africa with biparental brood care. After juvenile P. taeniatus have left their parents, they form loose shoals. Then, juveniles may have the option either to stay in their sibling group or to join a novel shoal. Therefore, in a first experiment, we tested whether juveniles prefer to shoal with their familiar sibling group or a group consisting of unfamiliar unrelated individuals. Second, we examined whether the shoaling decision translates into fitness benefits. We used body size as proxy for fitness and compared the growth in groups consisting exclusively of familiar full-siblings with growth in groups consisting of members of different relatedness and familiarity. Juvenile P. taeniatus preferred shoaling with kin over shoaling with non-kin. Growth was significantly higher in kin-only groups than in mixed groups indicating that grouping with familiar kin yields fitness benefits in juvenile P. taeniatus. Our results suggest that individual shoaling decisions based on social criteria can be adaptive.
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When faced with the presence of a predator, many species of prey initially approach rather than retreat from such a potential threat. The authors identify five major types of costs associated with approach behaviour: 1) increased risk of mortality to the approacher, 2) increased risk of mortality to relatives of the approacher, 3) lost opportunity costs associated with approaching a predator, 4) energetic costs of approach, and 5) potential costs of the approacher being "exploited' by other group members. Benefits of approach behaviour are: 1) acquiring information about the nature of the potential threat, 2) informing others of the potential threat, 3) deterring predator attack, and 4) advertising one's quality to mates. The authors present a game theory model of prey approaching potential predators. Based on the costs and benefits of approach behaviour and group size, the model predicts the equilibrial frequency of "approachers' and "non-approachers' and the (relative) mean approach distance (as a function of group size). -from Authors
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The social environment individuals are exposed to during ontogeny shapes social skills and social competence in groupliving animals. Consequently, social deprivation has serious effects on behaviour and development in animals but little is known about its impact on cooperation. In this study, we examined the effect of social environment on cooperative predator inspection. Predator inspection behaviour is a complex behaviour, which is present in a variety of shoaling fish species. Often, two fish leave the safety of the group and inspect a potentially dangerous predator in order to gather information about the current predation risk. As predator inspection is highly risky, it is prone to conflicts and cheating. However, cooperation among individuals may reduce the individual predation risk. We investigated this complex social behaviour in juveniles of the cichlid fish Pelvicachromis taeniatus that were reared in two different social environments throughout development. Fish reared in a group inspected more often than isolation-reared fish and were more likely to cooperate, i.e. they conducted conjoint inspection of a predator. By contrast, isolation-reared fish were more likely to perform a single inspection without a companion. These results suggest an impairment of cooperative behaviour in isolation-reared fish most probably due to lack of social experience and resulting in lowered social skills needed in coordinated behaviour.
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The evolution of alarm signals has puzzled evolutionary ecologists for decades. This is particularly true for alarm cues (‘Schreckstoff’) which are present in many fishes. They are passively released through injuries and signal the presence of a predator. Although the benefits for conspecific receivers are obvious (they can adjust their behavior to avoid predation), those for the senders are not which is, however, a necessary requirement for the evolution of alarm signals. Several hypotheses relying on potential direct benefits for the senders have been suggested. Alarm cues might attract secondary predators which in turn might increase the escape probability of the sender. A primary immune enhancing role was suggested as well. An alternative explanation is based on Hamilton’s inclusive fitness theory stating that individuals can indirectly increase their fitness by increasing the survival of genetically related individuals (‘kin selection theory’). If related individuals preferentially benefit from alarm signals, for instance by being more receptive to kin-alarm cues, senders could increase their inclusive fitness. Here, we investigate whether individuals of the cichlid fish Pelvicachromis taeniatus respond differentially to alarm cues derived from kin and non-kin. P. taeniatus possesses alarm cues and is known to adjust its behavior when exposed to alarm cues. We measured the change in activity after the addition of alarm cues (derived from kin- and non-kin) relative to a control treatment. Reduced activity is a widespread behavioral adaptation to reduce predation risk in prey organisms. Fish of the alarm cue treatments significantly reduced their activity relative to control fish. However, fish did not respond differentially to alarm cues derived from kin and non-kin suggesting that potential inclusive fitness benefits are not mediated by responses specific to individual alarm cues. We discuss alternative mechanisms such as kin-related grouping and mating preferences potentially leading to kin-biased alarm cue perception.
Inclusive fitness theory provides the conceptual framework for our current understanding of social evolution, and empirical studies suggest that kin selection is a critical process in the evolution of animal sociality. A key prediction of inclusive fitness theory is that altruistic behaviour evolves when the costs incurred by an altruist (c) are outweighed by the benefit to the recipient (b), weighted by the relatedness of altruist to recipient (r), i.e. Hamilton's rule rb > c. Despite its central importance in social evolution theory, there have been relatively few empirical tests of Hamilton's rule, and hardly any among cooperatively breeding vertebrates, leading some authors to question its utility. Here, we use data from a long-term study of cooperatively breeding long-tailed tits Aegithalos caudatus to examine whether helping behaviour satisfies Hamilton's condition for the evolution of altruism. We show that helpers are altruistic because they incur survival costs through the provision of alloparental care for offspring. However, they also accrue substantial benefits through increased survival of related breeders and offspring, and despite the low average relatedness of helpers to recipients, these benefits of helping outweigh the costs incurred. We conclude that Hamilton's rule for the evolution of altruistic helping behaviour is satisfied in this species.