LETTERS
Learning

torecognize

maladaptive
canorusArnonforcuckoo

nestlings

isCuculus

hosts

Lotem*

Departmentof Zoology, Faculty of Life Sciences,
Ramat Aviv, Tel Aviv 69978, Israel

Tel Aviv University,

THE picture of a tiny passerine host feeding a huge cuckoo nestlingchallenges evolutionary biologists who explain animal behaviour
as adaptivel-4. Cuckoo eggs sometimes resemble the eggs of thehost, but nestlings of the common cuckoo, Cuculus canorus, lookvery different from the young of the host. The inability of the hostto discriminate against such divergent nestlings is especiallypuzzling as so/ne cuckoo hosts show a finely tuned discrimination
ability between eggs5--8.Here I present a simple model to explain
this paradox. The model shows that although learning to recognize
eggs is adaptive, learning to recognize nestlings might not be. The
mechanism of learned recognition, previously shown to maintainegg recognition, is unlikely to be adaptive for hosts like those of
the common cuckoo, in which only the parasitic nestling remains
in the nest. The reason that discrimination against parasite nestlings is not adaptive is that the cost of misimprinting (learning torecognize the parasite nestling as the parents' own) exceeds thebenefit of correct learning. The model also explains why nestling
discrimination is mostly found in host-parasite systems in which
the parasite and the hosts' young are reared togetherl.
Recent studies indicate that cuckoos and their hosts may have
evolved several adaptations and counter adaptations to eachotherl.5.9.lo. Egg recognition is the common host defence against
cuckoo parasitism, but some level of acceptance of cuckoo eggsby hosts is also common6.8.9. Mimicry in cuckoo eggs and thecost of errors in egg recognition may prevent the parasitized
host from always rejecting the cuckoo eggs7. But because cuckoo
nestlings look different from the hosts' young, nestling discrimination should be easy. Soon after hatching, the cuckoo's nestlingejects all host eggs or nestlings from the nest. Although it isthus too late for the host to save its young, by deserting thecuckoo nestling a host can save about 30 days of parental carewhich might be used for renesting. It is therefore surprising thathosts have not developed nestling recognition by the samemechanism used for recognizing eggs.
Several studies suggest that egg recognition in birds is learnedby an imprinting-Iike process7.11-13,Accordingly, hosts imprint
on their own egg type during their first breeding attempt andlater will reject any different egg type. Given this ability, a hostshould be able to learn the appearance of its nestlings when it
first breeds, and use this knowledge to discriminate against
parasitic nestlings in future breeding attempts. B~t, as I show
below, learning to recognize nestlings is maladaptive for hosts
like those of the common cuckoo, for which only the parasitic
nestling survives in parasitized nests. Such hosts, if parasitized
during their first breeding attempt, will face only a parasitic
nestling during their learning period, and consequently wi1l
reject their own young in any future breeding attempt. In otherwords, the learning mechani~m may incur a cost, termed here
the 'misimprinting cost', which is the result of learning to recognize the wrong type of egg or nestling as 'own'. The fol1owing
model explores the effect of the misimprinting
cost on theevolution of egg recognition (Fig. I) and nestling recognition(Fig. 2) in a typical host of the common cuckoo (such as thegreat reed warbler, Acrocephalus arundinaceus ).
Each arrow in the model is label1ed with its probability of

TO NATURE

occurrence, and a payoff is listed at the end of each path. A
rejection strategy is adaptive if !Js overall payoff is greater thanthat of an acceptance strategy. In either case (egg or nestlingrecognition), if an acceptor is parasitized by a common cuckoo(a probability of P), its reproductive success is usually zeroI4.15,
and if it is not parasitized (probability of 1- P), its reproductive
success is on average equal to x (x > 0). As an acceptor, bydefinition, does not learn to discriminate, its payoff does notchange between its first breeding and the later breeding, and isconstantly equal to Po+ (1- P)x, which is (1- P)x. In general,the payoff of an acceptor will be n ( 1 -P)x, where n is thenumber of breeding cycles during a host lifetime.
The payoff for a rejecter is more complex and will be considered first for the case of egg recognition (Fig. 1). If a naive
rejecter is parasitized during its first breeding, there is a risk notonly that its payoff will be reduced to zero, but that it may also
learn to recognize the cuckoo egg, as well as the other eggs in
the clutch, as its own. Such an individual, if parasitized duringlater breeding attempts, might accept the cuckoo egg as its own,and consequently its payoff will be the same as that of anacceptor. However, if a rejecter is not parasitized in its firstbreeding and does learn to recognize its own type of eggs
correctly, and if it is parasitized in later breeding, it will gain
the benefit of rejection, designated as b. The payoff of a rejecter
is therefore PO+ P(n -1)(PO+(IP)x)+(I-P)x+(IP)(n-l)(Pb+(I-P)x),
which reduces to P(n-l)«I-P)x)+(I-P)x+(I-P)(n-l)(Pb+(I-P)x).
Accordingto themodel, and assuming that the parasitism rate is never 100%
(P < 1.0), a rejecter will do better than an acceptor as longas P(n-l)«IP)x) + (1- P)x+ (1- P)(n -1)(Pb + (1- P)x)
> n(l- P)x, which after solving, gives Pb > 0, or, put in words,
rejection is favoured as long as the population is parasitized(P>O) and that some benefits are gained by rejection (b>O).
Clearly, these are elementary conditions for the adaptiveness ofrejection per se, no matter what the rejection mechanism is.
Hence, despite the cost of misimprinting, the proposed learning
mechanism of egg recognition is adaptive.
The situation is different in the case of nestling recognition(Fig. 2). As in parasitized nests only the cuckoo nestling remains,a naive rejecter, if parasitized, may learn to recognize only theFirst breeding

Later breeding
payoffpayoffyAcceptor

oooe-;.

0/ooo.~o,,~oooo-;..x,,yooOI-;.

O~~0001-?0...~00000-?0X

Rejecter"~OOOO-;.X~

yooo~b...~oooo~XFIG, 1 The mechanism of learned egg recognition, for a typical host of acommon cuckoo (see text for explanation). P. the host probability of being
parasitized; ~ the average reproductive success (number of fledglings) of
a non-parasitized host; 0, zero' the reproductive success from a parasitized
nest; b, the benefit of egg rejection, which is the average reproduction
success of a parasitized host that rejects the cuckoo egg.

743

LETTERSTO NATURE

cuckoo nestling as its own. Such an individual will always accept
cuckoo nestlings when parasitized, but because it was not
exposed to its own young during the learning period, it will
reject them in later breeding attempts. Hence, the cost of misimprinting in this case is the loss of all future reproductive
success. Consideringthat cost, the payoff of a rejecter
will be PO+P(n-I)(PO+(I-P)O)+(I-P)x+(I-P)(n-l)(Pb+(I-P)x),
which
reduces toP(n-I)+(I-P)x+(1- P)(n -1)(Pb + (1- P)x). Assuming that 0 < P < I andx > 0, rejecters will do better than acceptors only if P(n -I) +(1- P)x + (1- P)(n -1)(Pb+ (1- P)x) > n(l- P)x, which after
solving, gives b > x. Put in words, rejecters will do better than
acceptors only if the benefit of nestling rejection ( b) is greaterthan the reproductive value of unparasitized nests (x). A situation like this probably never occurs; when rejection is achieved
by deserting the cuckoo nestling, the benefit of rejection is likely
to be lower than the value of an unparasitized nest because
renesting is not always possible, and even when it occurs, later
nests tend to have smaller clutches 16 and to lead to lower
reproductive successl7. The benefit of rejection might be higher
if the host can discriminate and eject the cuckoo nestling
immediately after it hatches, thus saving its own young. But
even if the host can save all its young ( b = x) rejection is no
better than acceptance. Moreover, because the cuckoo usually
removes one host egg when laying its ownl.15, the host still
remains with fewer nestlings than if it had not been parasitized( b < x ). In conclusion, the proposed learning mechanism cannot
be adaptive when the cuckoo nestling remains alone in the nest.
For simplicity, the model assumes equal probability of facinga cuckoo nestling in the first and in later breeding attempts. But
in cases in which experienced breeders are more likely to reject
cuckoo eggs7, they are inevitably less likely to face cuckoo
nestlings. Consequently, the probability of facing a cuckoo
nestling as a naive breeder, and thereby paying the cost ofmisimprinting, is greater than the probability of facing it as anexperienced breeder and then gaining the benefit of correct
learning. The likelihood of learned recognition being adaptiveis thus even less than that predicted by the model.
The cost of misimprinting is also relevant to cases where theparasite and the host nestling are reared together. If host nestlings frequently fail to compete for food with the parasite andFirst breeding

Later breeding

payoffpayoff~/'Acceptor~"[;;1"""0)'~"''\.. '.:0..!1~. 7 x~"q "£70~;1...':::"1 7 0.'.0"'-,. {'r:-:;;:;'~..~-.
,-

Rejecter~...~d7b~7X~H

FIG. 2 Hypothetical mechanism of learned nestling recognition, for a typicalhost of a common cuckoo (see text for explanation). P, the host probabilityof being parasitized; X, the average reproductive success (number offledglings) of a non-parasitized host: 0, zero: the reproductive success froma parasitized nest; b, the benefit of nestling rejection, which is the average
reproduction success of a parasitized host that rejects the cuckoo nestling.
744

starve to death, the cost of misimprinting may outweigh thebenefits of correct learning. On the other hand, if both host andparasite nestlings survive to fledging, learning to recognize nestlings should be adaptive. In agreement with this prediction,comparative evidence shows that nestling discriminationismostly found in host-parasite systems in which the parasite isreared along with the host young1 and causes little or no mortality among them9.18.19.Although more comparative evidenceof this kind can partially test the model, the mechanism of
nestling discrimination needs to be studied directly. The learning
hypothesis can be tested by experimentally replacing host nestlings with other nestling types during the host first breedingattempt. My model will be falsified if nestling discrimination is
exhibited by hosts in which only the parasitic nestling remains
in the nest, and if discrimination in this case is learned.
The model does not explain why hosts cannot recognize theirnestlings innately. But it is doubtful whether the common forms
of innate recognition could be sufficiently effective to reject asingle cuckoo nestling. An innate response to key releasers isoften stimulated by a broad range Qf stimuli that only slightly
resemble the 'correct' one2O.21.Animals may prefer the stronger
stimulus when faced with a simultaneous choice, but stillrespond to the weaker stimulus when it is the only one provided21. Such an innate preference may allow nestling discrimin!ltion where the parasite and the hosts' young are reared
together, but not in common cuckoo hosts where the parasite
remains alone. What is needed, but apparently does not exist,
is a genetic programme that allows the hosts to ignore all othersimilar stimuli, and to desert only the single cuckoo nestling.
The apparent lack of such a mechanism cannot serve as anexplanation, but should stimulate further research into innate
recognition and its limitations.
O

Received 2 December 1992; accepted 16 February 1993
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ACKNOWLfDGEl.£NTS I thank N Davies, A Erez, 0 Hasson, T Hatfield, H Nakamura, T Redond(), SRothstein, D Schluter, 1 Smith, D Ward and A Zahavi for comments and suggestions, This workwas supported by the United States-Israel Binational Science Foundation (BSF) and by an NSERC
postdoctorai

fellowship of the Canadian Government
NATURE.

VOl362.22

APRil1993