- Email: [email protected]
The cuckoo chick tricks their reed warbler foster parents, but what about other host species?
NEWS & COMMENT increase fitness in the context of fixed deleterious mutations. Burch and Chao’s experiment therefore also provides strong evidence that the fitness effects of alleles depend on their genetic background. In the context of mutational meltdown, these results are extremely encouraging. Although it has long been known that compensatory mutations could, for example, rescue some of the negative fitness consequences of visible mutations maintained in stock populations9,10, this is the first demonstration that this compensation can be so fast and so complete, even at small population sizes. Lande’s results demonstrate that back mutations alone can slow mutational meltdown substantially; Burch and Chao’s results show that mean fitness can increase, even at quite small population sizes, as a result of the potentially large number of ways in which evolution can achieve the same
fitness. Future experiments with other taxa and with other deleterious mutations would greatly increase our state of knowledge of the ways in which evolution can cope with the deleterious effects of mutation. Michael C. Whitlock Sarah P. Otto Department of Zoology, University of British Columbia, Vancouver, BC, Canada V6T 1Z4 ([email protected]; [email protected])
References 1 Drake, J.W. et al. (1998) Rates of spontaneous mutation, Genetics 148, 1667–1686 2 Lande, R. (1994) Risk of population extinction from fixation of new deleterious mutations, Evolution 48, 1460–1469 3 Lynch, M., Conery, J. and Bürger, R. (1995) Mutational meltdown in sexual populations, Evolution 49, 1067–1080
The cuckoo chick tricks their reed warbler foster parents, but what about other host species?
T
he picture of a small passerine perching on the shoulder of a monstrous European cuckoo (Cuculus canorus) chick and feeding it remains a fascinating evolutionary enigma1–3. Young cuckoos are very successful in eliciting food from their foster parents. A single cuckoo chick receives an amount of food equivalent to that of a brood of host young4, and its growth rate is also the same as that of the entire brood2. The puzzle of why chicks of parasitic cuckoos are so successful in obtaining food from their foster parents has been explained in different ways1,5–7. In a new paper, Kilner et al.8 provide novel insights into how the cuckoo chick tricks its reed warbler (Acrocephalus scirpaceus) hosts, with findings that raise intriguing questions*. Begging behaviour by nestlings involves directional stretching of the neck, wing shivering, gaping and calling, usually combined with gapes of exaggerated design and bright colouration. Such striking begging behaviour has recently received substantial attention from evolutionary biologists9–11, especially the *See Correspondence (p. 320) for comments on this article by R.M. Kilner, D.G. Noble and N.B. Davies.
296
problem of how parasitic chicks deceive their foster parents6,7,12. Parasitic cuckoos lay their eggs in the nests of other species, relying entirely on the foster parents to incubate the eggs and feed the chicks until independence. Thus, nestlings of brood parasites are attended by genetically unrelated individuals. Hence, the comparison of the begging behaviour of nestlings of parasitic and nonparasitic species can provide insight into the ways in which evolutionary forces shape begging behaviour. Kilner et al.8 studied the begging behaviour by which reed warbler chicks signal need to parents, and analysed cuckoo exploitation of this parent–offspring communication system. An initial analysis of the begging signals showed that both total gape area displayed by all chicks in the nest and begging call rate of broods of four reed warblers varied significantly with the duration of food deprivation. After the level of food deprivation was standardized by feeding chicks until satiation, nestlings were stimulated to beg every ten minutes. After 110 minutes the authors recorded the begging behaviour on video and audiotape, and quantified the amount of food consumed until begging ceased. This
0169-5347/99/$ – see front matter © 1999 Elsevier Science. All rights reserved.
4 Lynch, M., Conery, J. and Bürger, R. (1995) Mutation accumulation and the extinction of small populations, Am. Nat. 146, 489–518 5 Lande, R. (1995) Mutation and conservation, Conserv. Biol. 9, 782–791 6 Schultz, S.T. and Lynch, M. (1997) Mutation and extinction: the role of variable mutational effects, synergistic epistasis, beneficial mutations, and degree of outcrossing, Evolution 51, 1363–1371 7 Lande, R. (1998) Risk of population extinction from fixation of deleterious and reverse mutations, Genetica 102/103, 21–27 8 Burch, C.L. and Chao, L. (1999) Evolution by small steps and rugged landscapes in the RNA virus f6, Genetics 151, 921–927 9 Muller, H.J. (1939) Reversibility in evolution considered from the standpoint of genetics, Biol. Rev. 14, 261–280 10 Haldane, J.B.S. (1957) The cost of natural selection, J. Genet. 55, 511–524
amount was used as an indicator of the nestlings’ need. They found significant independent effects of each begging signal (gape area and begging rate) on the amount of food consumed, and an interaction effect of the two signals combined: both signals together provided parents with more accurate information about offspring need than either signal alone. Thus, the authors predicted that parents adjust the provisioning rate to both begging signals. Kilner et al.8 then tested this prediction by experimentally manipulating vocal signals (by broadcasting playbacks of begging calls near the nest or by manipulating brood size) and visual signals (by manipulating brood size). In support of their prediction, they found that the feeddelivery rate by both parents was independently affected by the maximum number of gapes displayed per nest and the maximum number of chicks calling per nest (the number of chicks in the brood plus the number of chicks calling on the playback tape). Thus, parents appear to regulate their provisioning rate according to multiple signals: the rate at which the brood calls and the total gape area displayed. Finally, the authors8 analysed the way in which the cuckoo chick exploits the parent–offspring communication system, according to how chicks signal their level of need and how parents adjust their provisioning rate by integrating visual and vocal nestling displays. Although the gape of the cuckoo chick is enormous compared with that of one reed warbler chick, Kilner et al. found that a single nestling cuckoo displays less gape area than a brood of four reed
PII: S0169-5347(99)01648-1
TREE vol. 14, no. 8 August 1999
NEWS & COMMENT warblers combined. This difference consistently increased as the single cuckoo chick and the brood of four reed warblers grew older. In contrast, when the cuckoo chick is six to eight days old, its rate of begging calls is very similar to that of a brood of four reed warblers, and with age its begging call becomes relatively even faster. The increasingly exuberant begging call of the young cuckoo could be explained as an adaptation to compensate for its diminishing gape area compared with the total gape area of a brood of four reed warblers8. This idea was tested using a regression equation [derived experimentally to relate begging signals to rate of parental provisioning: feeds delivered per hour 5 0.0162 (gape area displayed in mm2) 1 0.178 (calls per 6 s) 1 8.23] to predict begging call rate by the cuckoo chick at different ages. A comparison between predicted values and the cuckoo’s begging call rates recorded under natural conditions revealed no significant difference. This supports the idea that the increasing rate of begging calls by the growing cuckoo can be predicted from the cuckoo’s diminishing gape area (and hence relatively smaller stimulus) compared with that of the combined warbler brood. The key discovery is that the hosts follow exactly the same integration rule when feeding a single cuckoo as they do when feeding a brood of their own young. The study extends previous work by the same research group7, which found that week-old cuckoos trick their reedwarbler hosts by mimicking the begging calls of a brood of four host young. This new study8 poses the exciting conclusion that the cuckoo chick adjusts its begging display according to the sensory predisposition of the hosts; that is, to the stimuli that the hosts use to assess the nutritional need of their own offspring (the integration of both visual and vocal displays). The European cuckoo is an obligate brood parasite that has been recorded parasitizing nearly 100 species in Europe, although only 11 host species are parasitized frequently and about 12 occasionally2. Frequently used hosts differ in body size, from small passerines, such as the reed warbler (12 g), to the large redbacked shrike (Lanius collurio; 28.2 g) (Ref. 13). Kilner et al.8 have provided support for their idea about signal integration and concluded that the high rate of begging calls by the cuckoo chick in reed warbler nests is to compensate for a much smaller gape area than that of a whole host brood. Could this hypothesis also explain the success of the cuckoo chick in parasitizing other host TREE vol. 14, no. 8 August 1999
species? But the reed warbler is the smallest of the frequently used hosts of the European cuckoo2,13. Thus, given that cuckoo chicks display persistent vocal signals in reed warbler nests (5.6 calls per second)7, it is difficult to imagine how much more exaggerated the vocal display of a cuckoo chick should be to compensate for the gape area of a whole brood of a much larger host species, such as the red-backed shrike. Perhaps the relationship between vocal and visual display in the cuckoo chick is merely a coincidence, because in this small host species the cuckoo chick requires the foster parents to work at their maximum feeding capacity. Although the paper in Nature by Kilner et al. deals only with the link between cuckoo begging signals and host provisioning rules, considering the complete chain of events (chick need–begging signals–parent provisioning), we suggest that the exaggerated vocal begging of cuckoo chicks in reed warbler nests could be explained simply by taking into account that the cuckoo chick needs the same provisioning as an entire brood of reed warblers. For this reason the cuckoo chick solicits food at the same rate as that of a brood of reed warblers and, in fact, a cuckoo nestling receives the same rate of provisioning as a brood of reed warblers4,8. This idea is supported by the fact that the begging display of the cuckoo nestling is related to both its level of need and the willingness of the foster-parents to provide food; that is, during the first days of the nestling period, the cuckoo chick does not produce begging calls at all because the quantity of food needed by the single cuckoo chick is easily provided by both foster parents. However, the begging rate of the cuckoo chick when six to eight days old resembles that of a brood of four reed warblers, and steadily accelerates with age8, because the amount of food required by the cuckoo chick is close to the maximum feeding capacity of the reed-warbler foster parents. Kilner et al.8 do not discuss how their hypothesis affects other larger host species. However, our hypothesis, that the begging rate of the cuckoo chick is in accordance with its level of need and/or with the feeding capacity of the foster parents, predicts that the cuckoo vocal display should be less exaggerated in species of larger size because of their higher capacity to provision food. However, another possibility is that cuckoo vocal displays might always be the same (very exaggerated as in reed warbler nests, adapted to the host species of smaller size), regardless of the host size. Further experimental studies on the
begging behaviour of cuckoo and host chicks when parasitizing host species of different size are needed. Kilner et al. have shown the way in which this can be done. Acknowledgements We are grateful to N.B. Davies, Rebecca Kilner, Anders Møller and D.G. Noble for comments on the manuscript. Financial support was given by the DGICYT PB94-0785 research project.
Manuel Soler Juan José Soler Departamento de Biología Animal y Ecología, Facultad de Ciencias, Universidad de Granada, E-18071 Granada, Spain ([email protected])
References 1 Dawkins, R. and Krebs, J.R. (1979) Arms races between and within species, Proc. R. Soc. London Ser. B 205, 489–511 2 Wyllie, I. (1981) The Cuckoo, B.T. Batsford 3 Davies, N.B. and Brooke, M. de L. (1989) An experimental study of co-evolution between the cuckoo, Cuculus canorus, and its hosts. II. Host egg markings, chick discrimination and general discussion, J. Anim. Ecol. 58, 225–236 4 Brooke, M. de L. and Davies, N.B. (1989) Provisioning of nestling cuckoos Cuculus canorus by reed warbler Acrocephalus scirpaceus hosts, Ibis 131, 250–256 5 Soler, M. et al. (1995) Preferential allocation of food by magpies Pica pica to great spotted cuckoo Clamator glandarius chicks, Behav. Ecol. Sociobiol. 37, 7–13 6 Lichtenstein, G. and Sealy, S.G. (1998) Nestling competition, rather than supernormal stimulus, explains the success of parasitic brown-headed cowbird chicks in yellow warbler nests, Proc. R. Soc. London Ser. B 265, 249–254 7 Davies, N.B., Kilner, R.M. and Noble, D.G. (1998) Nestling cuckoos, Cuculus canorus, exploit hosts with begging calls that mimic a brood, Proc. R. Soc. London Ser. B 265, 673–678 8 Kilner, R.M., Noble, D.G. and Davies, N.B. (1999) Signals of need in parent–offspring communication and their exploitation by the common cuckoo, Nature 397, 667–672 9 Godfray, H.C.J. (1995) Signalling of need between parents and young: parent–offspring conflict and sibling rivalry, Am. Nat. 146, 1–24 10 Kilner, R. and Johnstone, R.A. (1997) Begging the question: are offspring solicitation behaviours signals of need? Trends Ecol. Evol. 12, 11–15 11 Lotem, A. (1998) Differences in begging behaviour between barn swallow, Hirundo rustica, nestlings, Anim. Behav. 55, 809–818 12 Dearborn, D.C. (1998) Begging behavior and food acquisition by brown-headed cowbird nestlings, Behav. Ecol. Sociobiol. 43, 259–270 13 Perrins, C. (1988) Aves de España y de Europa (Nueva generación de guías), Omega
297
fitness. Future experiments with other taxa and with other deleterious mutations would greatly increase our state of knowledge of the ways in which evolution can cope with the deleterious effects of mutation. Michael C. Whitlock Sarah P. Otto Department of Zoology, University of British Columbia, Vancouver, BC, Canada V6T 1Z4 ([email protected]; [email protected])
References 1 Drake, J.W. et al. (1998) Rates of spontaneous mutation, Genetics 148, 1667–1686 2 Lande, R. (1994) Risk of population extinction from fixation of new deleterious mutations, Evolution 48, 1460–1469 3 Lynch, M., Conery, J. and Bürger, R. (1995) Mutational meltdown in sexual populations, Evolution 49, 1067–1080
The cuckoo chick tricks their reed warbler foster parents, but what about other host species?
T
he picture of a small passerine perching on the shoulder of a monstrous European cuckoo (Cuculus canorus) chick and feeding it remains a fascinating evolutionary enigma1–3. Young cuckoos are very successful in eliciting food from their foster parents. A single cuckoo chick receives an amount of food equivalent to that of a brood of host young4, and its growth rate is also the same as that of the entire brood2. The puzzle of why chicks of parasitic cuckoos are so successful in obtaining food from their foster parents has been explained in different ways1,5–7. In a new paper, Kilner et al.8 provide novel insights into how the cuckoo chick tricks its reed warbler (Acrocephalus scirpaceus) hosts, with findings that raise intriguing questions*. Begging behaviour by nestlings involves directional stretching of the neck, wing shivering, gaping and calling, usually combined with gapes of exaggerated design and bright colouration. Such striking begging behaviour has recently received substantial attention from evolutionary biologists9–11, especially the *See Correspondence (p. 320) for comments on this article by R.M. Kilner, D.G. Noble and N.B. Davies.
296
problem of how parasitic chicks deceive their foster parents6,7,12. Parasitic cuckoos lay their eggs in the nests of other species, relying entirely on the foster parents to incubate the eggs and feed the chicks until independence. Thus, nestlings of brood parasites are attended by genetically unrelated individuals. Hence, the comparison of the begging behaviour of nestlings of parasitic and nonparasitic species can provide insight into the ways in which evolutionary forces shape begging behaviour. Kilner et al.8 studied the begging behaviour by which reed warbler chicks signal need to parents, and analysed cuckoo exploitation of this parent–offspring communication system. An initial analysis of the begging signals showed that both total gape area displayed by all chicks in the nest and begging call rate of broods of four reed warblers varied significantly with the duration of food deprivation. After the level of food deprivation was standardized by feeding chicks until satiation, nestlings were stimulated to beg every ten minutes. After 110 minutes the authors recorded the begging behaviour on video and audiotape, and quantified the amount of food consumed until begging ceased. This
0169-5347/99/$ – see front matter © 1999 Elsevier Science. All rights reserved.
4 Lynch, M., Conery, J. and Bürger, R. (1995) Mutation accumulation and the extinction of small populations, Am. Nat. 146, 489–518 5 Lande, R. (1995) Mutation and conservation, Conserv. Biol. 9, 782–791 6 Schultz, S.T. and Lynch, M. (1997) Mutation and extinction: the role of variable mutational effects, synergistic epistasis, beneficial mutations, and degree of outcrossing, Evolution 51, 1363–1371 7 Lande, R. (1998) Risk of population extinction from fixation of deleterious and reverse mutations, Genetica 102/103, 21–27 8 Burch, C.L. and Chao, L. (1999) Evolution by small steps and rugged landscapes in the RNA virus f6, Genetics 151, 921–927 9 Muller, H.J. (1939) Reversibility in evolution considered from the standpoint of genetics, Biol. Rev. 14, 261–280 10 Haldane, J.B.S. (1957) The cost of natural selection, J. Genet. 55, 511–524
amount was used as an indicator of the nestlings’ need. They found significant independent effects of each begging signal (gape area and begging rate) on the amount of food consumed, and an interaction effect of the two signals combined: both signals together provided parents with more accurate information about offspring need than either signal alone. Thus, the authors predicted that parents adjust the provisioning rate to both begging signals. Kilner et al.8 then tested this prediction by experimentally manipulating vocal signals (by broadcasting playbacks of begging calls near the nest or by manipulating brood size) and visual signals (by manipulating brood size). In support of their prediction, they found that the feeddelivery rate by both parents was independently affected by the maximum number of gapes displayed per nest and the maximum number of chicks calling per nest (the number of chicks in the brood plus the number of chicks calling on the playback tape). Thus, parents appear to regulate their provisioning rate according to multiple signals: the rate at which the brood calls and the total gape area displayed. Finally, the authors8 analysed the way in which the cuckoo chick exploits the parent–offspring communication system, according to how chicks signal their level of need and how parents adjust their provisioning rate by integrating visual and vocal nestling displays. Although the gape of the cuckoo chick is enormous compared with that of one reed warbler chick, Kilner et al. found that a single nestling cuckoo displays less gape area than a brood of four reed
PII: S0169-5347(99)01648-1
TREE vol. 14, no. 8 August 1999
NEWS & COMMENT warblers combined. This difference consistently increased as the single cuckoo chick and the brood of four reed warblers grew older. In contrast, when the cuckoo chick is six to eight days old, its rate of begging calls is very similar to that of a brood of four reed warblers, and with age its begging call becomes relatively even faster. The increasingly exuberant begging call of the young cuckoo could be explained as an adaptation to compensate for its diminishing gape area compared with the total gape area of a brood of four reed warblers8. This idea was tested using a regression equation [derived experimentally to relate begging signals to rate of parental provisioning: feeds delivered per hour 5 0.0162 (gape area displayed in mm2) 1 0.178 (calls per 6 s) 1 8.23] to predict begging call rate by the cuckoo chick at different ages. A comparison between predicted values and the cuckoo’s begging call rates recorded under natural conditions revealed no significant difference. This supports the idea that the increasing rate of begging calls by the growing cuckoo can be predicted from the cuckoo’s diminishing gape area (and hence relatively smaller stimulus) compared with that of the combined warbler brood. The key discovery is that the hosts follow exactly the same integration rule when feeding a single cuckoo as they do when feeding a brood of their own young. The study extends previous work by the same research group7, which found that week-old cuckoos trick their reedwarbler hosts by mimicking the begging calls of a brood of four host young. This new study8 poses the exciting conclusion that the cuckoo chick adjusts its begging display according to the sensory predisposition of the hosts; that is, to the stimuli that the hosts use to assess the nutritional need of their own offspring (the integration of both visual and vocal displays). The European cuckoo is an obligate brood parasite that has been recorded parasitizing nearly 100 species in Europe, although only 11 host species are parasitized frequently and about 12 occasionally2. Frequently used hosts differ in body size, from small passerines, such as the reed warbler (12 g), to the large redbacked shrike (Lanius collurio; 28.2 g) (Ref. 13). Kilner et al.8 have provided support for their idea about signal integration and concluded that the high rate of begging calls by the cuckoo chick in reed warbler nests is to compensate for a much smaller gape area than that of a whole host brood. Could this hypothesis also explain the success of the cuckoo chick in parasitizing other host TREE vol. 14, no. 8 August 1999
species? But the reed warbler is the smallest of the frequently used hosts of the European cuckoo2,13. Thus, given that cuckoo chicks display persistent vocal signals in reed warbler nests (5.6 calls per second)7, it is difficult to imagine how much more exaggerated the vocal display of a cuckoo chick should be to compensate for the gape area of a whole brood of a much larger host species, such as the red-backed shrike. Perhaps the relationship between vocal and visual display in the cuckoo chick is merely a coincidence, because in this small host species the cuckoo chick requires the foster parents to work at their maximum feeding capacity. Although the paper in Nature by Kilner et al. deals only with the link between cuckoo begging signals and host provisioning rules, considering the complete chain of events (chick need–begging signals–parent provisioning), we suggest that the exaggerated vocal begging of cuckoo chicks in reed warbler nests could be explained simply by taking into account that the cuckoo chick needs the same provisioning as an entire brood of reed warblers. For this reason the cuckoo chick solicits food at the same rate as that of a brood of reed warblers and, in fact, a cuckoo nestling receives the same rate of provisioning as a brood of reed warblers4,8. This idea is supported by the fact that the begging display of the cuckoo nestling is related to both its level of need and the willingness of the foster-parents to provide food; that is, during the first days of the nestling period, the cuckoo chick does not produce begging calls at all because the quantity of food needed by the single cuckoo chick is easily provided by both foster parents. However, the begging rate of the cuckoo chick when six to eight days old resembles that of a brood of four reed warblers, and steadily accelerates with age8, because the amount of food required by the cuckoo chick is close to the maximum feeding capacity of the reed-warbler foster parents. Kilner et al.8 do not discuss how their hypothesis affects other larger host species. However, our hypothesis, that the begging rate of the cuckoo chick is in accordance with its level of need and/or with the feeding capacity of the foster parents, predicts that the cuckoo vocal display should be less exaggerated in species of larger size because of their higher capacity to provision food. However, another possibility is that cuckoo vocal displays might always be the same (very exaggerated as in reed warbler nests, adapted to the host species of smaller size), regardless of the host size. Further experimental studies on the
begging behaviour of cuckoo and host chicks when parasitizing host species of different size are needed. Kilner et al. have shown the way in which this can be done. Acknowledgements We are grateful to N.B. Davies, Rebecca Kilner, Anders Møller and D.G. Noble for comments on the manuscript. Financial support was given by the DGICYT PB94-0785 research project.
Manuel Soler Juan José Soler Departamento de Biología Animal y Ecología, Facultad de Ciencias, Universidad de Granada, E-18071 Granada, Spain ([email protected])
References 1 Dawkins, R. and Krebs, J.R. (1979) Arms races between and within species, Proc. R. Soc. London Ser. B 205, 489–511 2 Wyllie, I. (1981) The Cuckoo, B.T. Batsford 3 Davies, N.B. and Brooke, M. de L. (1989) An experimental study of co-evolution between the cuckoo, Cuculus canorus, and its hosts. II. Host egg markings, chick discrimination and general discussion, J. Anim. Ecol. 58, 225–236 4 Brooke, M. de L. and Davies, N.B. (1989) Provisioning of nestling cuckoos Cuculus canorus by reed warbler Acrocephalus scirpaceus hosts, Ibis 131, 250–256 5 Soler, M. et al. (1995) Preferential allocation of food by magpies Pica pica to great spotted cuckoo Clamator glandarius chicks, Behav. Ecol. Sociobiol. 37, 7–13 6 Lichtenstein, G. and Sealy, S.G. (1998) Nestling competition, rather than supernormal stimulus, explains the success of parasitic brown-headed cowbird chicks in yellow warbler nests, Proc. R. Soc. London Ser. B 265, 249–254 7 Davies, N.B., Kilner, R.M. and Noble, D.G. (1998) Nestling cuckoos, Cuculus canorus, exploit hosts with begging calls that mimic a brood, Proc. R. Soc. London Ser. B 265, 673–678 8 Kilner, R.M., Noble, D.G. and Davies, N.B. (1999) Signals of need in parent–offspring communication and their exploitation by the common cuckoo, Nature 397, 667–672 9 Godfray, H.C.J. (1995) Signalling of need between parents and young: parent–offspring conflict and sibling rivalry, Am. Nat. 146, 1–24 10 Kilner, R. and Johnstone, R.A. (1997) Begging the question: are offspring solicitation behaviours signals of need? Trends Ecol. Evol. 12, 11–15 11 Lotem, A. (1998) Differences in begging behaviour between barn swallow, Hirundo rustica, nestlings, Anim. Behav. 55, 809–818 12 Dearborn, D.C. (1998) Begging behavior and food acquisition by brown-headed cowbird nestlings, Behav. Ecol. Sociobiol. 43, 259–270 13 Perrins, C. (1988) Aves de España y de Europa (Nueva generación de guías), Omega
297