Abstract
Interspecific brood parasites may use the secondary sexual characters of the hosts to decide which species to parasitize. Hence, species with conspicuous and well-recognisable traits may have higher chances of becoming parasitised. Using North American birds and their frequent brood parasite, the brown-headed cowbird Molothrus ater, we tested the relationship between features of song and plumage coloration of hosts and the frequency of brood parasitism while controlling for several potentially confounding factors. Relying on two sets of analysis, we focused separately on the evolutionary view of the parasite and the host. From the cowbird’s perspective, we found that males of heavily parasitized species posit songs with low syllable repertoire size, shorter inter-song interval and have brighter plumage. From the host’s perspective, a phylogenetic analysis revealed similar associations for features of song, but not for plumage characteristics that were unrelated to brood parasitism. These comparative findings may imply that brood parasites choose novel hosts based on heterospecific signals; and/or host species working against sexual selection escape from brood parasitism by evolving inconspicuous sexual signals. Although our data do not allow us to distinguish between these two evolutionary scenarios, our results suggest that selection factors mediating cowbird parasitism via host recognition by heterospecific signals may have an important role in the evolutionary relationship between brood parasites and their hosts.
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References
Andersson M (1994) Sexual selection. Princeton University Press, Princeton, N.J.
Andersson S, Amundsen T (1997) Ultraviolet colour vision and ornamentation in bluethroats. Proc R Soc Lond Ser B 264:1587–1591
Banks AJ, Martin TE (2001) Host activity and the risk of nest parasitism by brown-headed cowbirds. Behav Ecol 12:31–40
Bennett PM, Owens IPF (2002) Evolutionary ecology of birds. Oxford University Press, Oxford
Bennett ATD, Cuthill IC, Norris K (1994) Sexual selection and the mismeasure of color. Am Nat 144:848–860
Bennett ATD, Cuthill IC, Partridge JC, Maier EJ (1996) Ultraviolet vision and mate choice in zebra finches. Nature 380:433–435
Birkhead TR, Møller AP (1998) Sperm competition and sexual selection. Academic Press, London
Briskie JV, Sealy SG, Hobson KA (1992) Behavioral defenses against avian brood parasitism in sympatric and allopatric host populations. Evolution 46:334–340
Catchpole CK, Slater PJB (1995) Bird song: biological themes and variations. Cambridge University Press, Cambridge
Cuthill IC, Partridge JC, Bennett ATD, Church SC, Hart NS, Hunt S (2000) Ultraviolet vision in birds. Adv Study Behav 29:159–214
Davies NB, Brooke MD (1988) Cuckoos versus reed warblers-adaptation and counteradaptations. Anim Behav 36:262–284
Dunning JJB (1993) Handbook of avian body masses. CRC, Ann Arbor
Eastzer D, Chu PR, King AP (1980) The young cowbird—average or optimal nestling. Condor 82:417–425
Endler JA (1992) Signals, signal conditions and the direction of evolution. Am Nat 139:S125–S153
Endler JA (1993) Some general comments on the evolution and design of animal signalling systems. Philos Trans R Soc Lond B 340:215–225
Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15
Friedmann H (1929) The cowbirds: a study in the biology of social parasitism. Thomas, Springfield, Baltimore, Md.
Friedmann H, Kiff LF (1985) The parasitic cowbirds and their hosts. Proc Western Found Vert Zool 2:225–302
Garamszegi LZ, Møller AP (2004) Extra-pair paternity and the evolution of bird song. Behav Ecol 15:508–519
Garamszegi LZ, Møller AP, Erritzøe J (2003) The evolution of immune defense and song complexity in birds. Evolution 57:905–912
Grapputo A, Pilastro A, Baker AJ, Martin G (2001) Molecular evidence for phylogenetic relationships among buntings and American sparrows (Emberizidae). J Avian Biol 32:95–101
Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites. Science 218:384–387
Harvey PH, Pagel MD (1991) The comparative method in evolutionary biology. Oxford University Press, Oxford
Hauber ME, Pearson HE, Reh A, Merges A (2002) Discrimination between host songs by brood parasitic brown-headed cowbirds (Molothrus ater). Anim Cogn 5:129–137
Hosoi SA, Rothstein SI (2000) Nest desertion and cowbird parasitism: evidence for evolved responses and evolutionary lag. Anim Behav 59:823–840
Johnson KP, Lanyon SM (1999) Molecular systematics of the grackles and allies, and the effect of additional sequence (cyt b and ND2). Auk 116:759–768
Kilner RM (2003) How selfish is a cowbird nestling? Anim Behav 66:569–576
Klicka J, Johnson KP, Lanyon SM (2000) New world nine-primaried oscine relationships: constructing a mitochondrial DNA framework. Auk 117:321–336
Kozlovic DR, Knapton RW, Barlow JC (1996) Unsuitability of the house finch as a host of the brown-headed cowbird. Condor 98:253–258
Krüger O, Davies NB (2002) The evolution of cuckoo parasitism: a comparative analysis. Proc R Soc Lond Ser B 269:375–381
Lorenzana JC, Sealy SG (1999) A meta-analysis of the impact of parasitism by the brown-headed cowbird on its hosts. Studies Avian Biol 18:241–253
Lovette IJ, Bermingham E (2002) What is wood-warbler? Molecular characterisation of a monophyletic Parulidae. Auk 119:695–714
Lowther PE (1993) Brown-headed cowbird, Molothrus ater. In: Poole A, Stettenheim P, Gill F (eds) The birds of North America, vol 47. American Ornitologists’ Union, Philadelphia, Pa.
Møller AP (1991) Why mated songbirds sing so much: mate guarding and male announcement of mate fertility status. Am Nat 138:994–1014
Møller AP, Birkhead TR (1994) The evolution of plumage brightness in birds is related to extrapair paternity. Evolution 48:1089–1100
Møller AP, Pomiankowski A (1993) Punctuated equilibria or gradual evolution: the importance of fluctuating asymmetry. J Theor Biol 161:359–367
MacDougall-Shackleton SA (1997) Sexual selection and the evolution of song repertoires. In: Nolan V, Ketterson ED, Thompson CF (eds) Current ornithology, vol 14. Plenum, New York, pp 81–124
Martínez JG, Soler JJ, Soler M, Møller AP, Burke T (1999) Comparative population structure and gene flow of a brood parasite, the great spotted cuckoo (Clamator glandarius), and its primary host, the magpie (Pica pica). Evolution 53:269–278
Mayfield H (1965) The brown-headed cowbird with old and new hosts. Living Bird 4:13–28
National Geographic Society (2000) Field guide to the birds of North America. National Geographic Society, Washington, D.C.
Orians GH, Røskaft E, Beletsky LD (1989) Do brown-headed cowbirds lay their eggs at random in the nest of red-winged blackbirds? Wilson Bull 101:599–605
Ortega CP (1998) Cowbirds and other brood parasites. Univesity of Arizona Press, Tucson, Ariz.
Øien IJ, Moksnes A, Røskaft E (1995) Evolution of variation in egg color and marking pattern in european passerines—adaptations in a coevolutionary arms-race with the cuckoo, Cuculus canorus. Behav Ecol 6:166–174
Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–884
Payne RB, Payne LL, Woods JL, Sorenson MD (2000) Imprinting and the origin of parasite-host species associations in brood-parasitic indigobirds, Vidua chalybeata. Anim Behav 59:69–81
Petit LJ (1991) Adaptive tolerance of cowbird parasitism by prothonotary warblers—a consequence of nest-site limitation. Anim Behav 41:425–432
Poole A, Stettenheim P, Gill F (eds) (1993–2002) The birds of North America. American Ornitologists’ Union, Academy of Natural Sciences of Philadelphia, Philadelphia, Pa.
Purvis A, Rambaut A (1995) Comparative analysis by independent contrasts (CAIC): An Apple Macintosh application for analysing comparative data. Comp Appl Biosci 11:247–251
Røskaft E, Orians GH, Beletsky LD (1990) Why do red-winged blackbirds accept eggs of brown-headed cowbirds? Evol Ecol 4:35–42
Røskaft E, Moksnes A, Stokke BG, Moskát C, Honza M (2002) The spatial habitat structure of host populations explains the pattern of rejection behavior in hosts and parasitic adaptations in cuckoos. Behav Ecol 13:163–168
Read AF, Weary DM (1992) The evolution of bird song: comparative analyses. Philos Trans R Soc Lond B 338:165–187
Richards DG (1981) Environmental acoustics and censuses of singing birds. Stud Avian Biol 6:297–300
Rothstein SI (1975) An experimental and teleonomic investigation of avian brood parasitism. Condor 77:250–271
Rothstein SI (1990) A model system for coevolution: avian brood parasitism. Annu Rev Ecol Syst 21:481–508
Rothstein SI (1994) The cowbird’s invasion of the far west: history, causes and consequences experienced by host species. Stud Avian Biol 15:301–305
Rothstein SI, Robinson SK (1998) The evolution and ecology of avian brood parasites. In: Rothstein SI, Robinson SK (eds) Parasitic birds and their hosts: studies in coevolution, vol 9. Oxford University Press, Oxford, pp 3–56
Ryan MJ, Brenowitz EA (1985) The role of body size, phylogeny, and ambient noise in the evolution of bird song. Am Nat 126:87–100
Sibley CG, Ahlquist JE (1990) Phylogeny and classification of birds: a study in molecular evolution. Yale University Press, New Haven, Conn.
Slabbekoorn H, Smith TB (2002) Bird song, ecology, and speciation. Philos Trans R Soc Lond B 357:493–503
Sokal RR, Rohlf FJ (1995) Biometry 3rd edn. Freeman, New York
Soler M, Møller AP (1990) Duration of sympatry and coevolution between the great spotted cuckoo and its magpie host. Nature 343:748–750
Soler M, Møller AP (1996) A comparative analysis of the evolution of variation in appearance of eggs of European passerines in relation to brood parasitism. Behav Ecol 7:89–94
Soler JJ, Soler M, Møller AP, Martínez JG (1995) Does the great spotted cuckoo choose magpie host according to their parenting ability? Behav Ecol Sociobiol 36:201–206
Soler JJ, Martínez JG, Soler M, Møller AP (1999) Host sexual selection and cuckoo parasitism: an analysis of nest size in sympatric and allopatric magpie Pica pica populations parasitized by the great spotted cuckoo Clamator glandarius. Proc R Soc Lond B 266:1765–1771
Soler JJ, Martínez JG, Soler M, Møller AP (2001) Life history of magpie populations sympatric or allopatric with the brood parasitic great spotted cuckoo. Ecology 82:1621–1631
Spaw CD, Rohwer S (1987) A Comparative study of eggshell thickness in cowbirds and other passerines. Condor 89:307–318
Stokke BG, Moksnes A, Røskaft E (2002) Obligate brood parasites as selective agents for evolution of egg appearance in passerine birds. Evolution 56:199–205
Trine CL, Robinson D, Robinson SK (1998) Consequences of brown-headed cowbird brood parasitism for host population dynamics. In: Rothstein SI, Robinson SK (eds) Parasitic birds and their hosts: studies in coevolution, vol 9. Oxford University Press, Oxford, pp 273–295
Uyehara JC, Narins PM (1995) Nest defense by willow flycatchers to brood-parasitic intruders. Condor 97:361–368
Wiley RH (1983) The evolution of communication: information and manipulation. In: Halliday TR, Slater PJB (eds) Communication. Blackwell, Oxford, pp 82–113
Wiley RH (1991) Associations of song properties with habitats for territorial oscine birds of Eastern North America. Am Nat 134:973–993
Wiley RH (1992) Errors, exaggeration and deception in animal communication. In: Real LA (ed) Behavioural mechanisms in evolutionary ecology. University of Chicago Press, London, pp 157–189
Wiley RH, Richards DJ (1978) Physical constraints on acoustic communication in the atmosphere: implications for the evolution of animal vocalizations. Behav Ecol Sociobiol 3:69–94
Woolfenden BE, Gibbs HL, Sealy SG, McMaster DG (2003) Host use and fecundity of individual female brown-headed cowbirds. Anim Behav 58:895–905
Wyllie I (1981) The cuckoo. Batsford, London
Acknowledgements
We would like to thank J. Ewen, J. J. Soler and three anonymous referees for their constructive comments. M. Eens and B. Gunnar Stokke provided useful remarks on a previous version of this manuscript. B. Gunnar Stokke kindly helped to collect some data on brood parasitism. We are also grateful to M. Eens for scoring plumage coloration. L. Z. G. was supported by a postdoctoral grant from the FWO-Flanders (Belgium).
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Garamszegi, L.Z., Avilés, J.M. Brood parasitism by brown-headed cowbirds and the expression of sexual characters in their hosts. Oecologia 143, 167–177 (2005). https://doi.org/10.1007/s00442-004-1784-z
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DOI: https://doi.org/10.1007/s00442-004-1784-z