Kinship reinforces cooperative predator inspection in a cichlid fish

Abstract

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.

Full text

Kinship reinforces cooperative predator inspection in a
cichlid fish
SASKIA HESSE*, JAIME M. ANAYA-ROJAS*†‡,JOACHIMG.FROMMEN§&
TIMO TH
€
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
Keywords:
cooperation;
inclusive fitness;
kin recognition;
kin selection;
predation;
tit for tat.
Abstract
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.
Introduction
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:
shesse@evolution.uni-bonn.de
Data Archival Location: Attached to this file as supplementary
information.
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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 &
Akc
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€
oglund
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
behaviour.
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
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2S. HESSE ET AL.

P. taeniatus prefer shoaling with their kin (Th€
unken
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.
Predators
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
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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
once.
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€
ıve
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
2
=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.
Predator
compartment
Acclimasaon
compartment
Experimental compartment
Inspecon
zone
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.
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4S. HESSE ET AL.

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.
Results
Kinship explained differences in time test fish spent in
cooperative inspections (LME, LRT: v
2
=10.614,
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
2
=15.305, d.f. =1,
P<0.001), whereas body size difference (LME, LRT:
v
2
=1.783, d.f. =1, P=0.182) and number of defec-
tions (LME, LRT: v
2
=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
kin
SD =40.385s 61.134,
mean
nonkin
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
kin
SD =0.885 0.860, mean
non
kin
SD =1.192 1.182; Wilcoxon rank sum test,
W=72.5, P=0.542).
Discussion
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
***
400
350
300
250
200
150
100
50
Time (s) spent in cooperave inspecons
0
Kin Non kin
Fig. 2 Mean time SE (s) test fish spent in cooperative
inspections during the trial (total time: 400 s). ***Indicates
P=0.001.
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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
individuals.
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 &
Th€
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
interest.
Funding
This work was supported by a grant of the Deutsche
Forschungsgemeinschaft (TH 1516/1-1).
Acknowledgments
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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Supporting information
Additional Supporting Information may be found in the
online version of this article:
Data S1 Supporting information.
Received 24 February 2015; revised 17 June 2015; accepted 28 July
2015
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