Chinese Birds
Chinese Birds 2012, 3(4) 259-273 DOI:   10.5122/cbirds.2012.0033  ISSN: 1674-7674 CN: 11-5870/Q

Current Issue | Archive | Search                                                            [Print]   [Close]
REVIEW

Information and Service
This Article
Supporting info
PDF(1469KB)
[HTML]
Reference
Service and feedback
Email this article to a colleague
Add to Bookshelf
Add to Citation Manager
Cite This Article
Email Alert
Keywords
abiotic environment
biotic environment
coevolution
cuckoos
geographic theory of coevolution
life history traits
limits to adaptation
Authors
Anders P. MOLLER
Juan J. SOLER
PubMed
Article by Anders P. MOLLER
Article by Juan J. SOLER

A coevolutionary framework based on temporal and spatial ecology of host-parasite interactions: A missing link in studies of brood parasitism

Anders P. MOLLER 1,*, Juan J. SOLER 2

1 Laboratoire d’Ecologie, Systématique et Evolution, CNRS UMR 8079, Université Paris-Sud, Bâtiment 362, F-91405 Orsay Cedex, France 2 Estación Experimental de Zonas Áridas, Ctra. Sacramento s/n, La Cañada de San Urbano, E-04120 Almería, Spain

Abstract

A central tenet of coevolutionary theory, including theory of the coevolutionary relationship between brood parasites and their hosts, is that temporal and spatial patterns may reveal important information about ecological and evolutionary dynamics. For instance, level of genetic structure of populations provides important information about the role of genetics and gene flow in determining local patterns of selection on hosts due to parasitism (i.e., egg rejection) and on parasites due to selection by hosts (i.e., egg mimicry). Furthermore, abiotic (i.e., climatic conditions) and biotic (phenotypic characteristics of animals) factors that also vary spatially may directly or indirectly affect populations of hosts and brood parasites and, therefore, their interaction. By reviewing the literature, we found considerable evidence for an effect of the spatially and temporally structured abiotic environment on the phenotype of both parasite and host eggs and the degree of mimicry. Moreover, we found examples suggesting that specific life history characteristics of hosts that vary geographically and/or temporally may affect the probability of initial colonization of a new host species and the direction and the speed of coevolution. We provide an exhaustive review of studies investigating temporal and spatial patterns of the interaction between brood parasites and their hosts. Such temporal and spatial trends in parasite and host traits are, together with genetic information on rejection and significant effects of gene flow, consistent with coevolutionary dynamics. However, gene flow and changes in the temporal and spatial patterns of abundance of both parasites and hosts may result in frequent cases of counter-intuitive relationships between the phenotype of the parasite and that of the host (i.e., poor or no mimicry), which may suggest limits to the degree of adaptation. We provide a list of scientific questions in need of further investigation, concluding that studies of brood parasites and their hosts may play a central role in testing the geographic theory of coevolution and several alternative hypotheses.

Keywords abiotic environment   biotic environment   coevolution   cuckoos   geographic theory of coevolution   life history traits   limits to adaptation  
Received 2012-10-11 Revised 2012-11-30 Online:  
DOI: 10.5122/cbirds.2012.0033
Corresponding Authors: Anders P. Moller
Email: anders.moller@u-psud.fr
About author:

References:
Avilés JM, Stokke BG, Moksnes A, Røskaft E, Asmul M, Møller AP. 2006. Rapid increase in cuckoo egg matching in a recently parasitized reed warbler population. J Evol Biol, 19:1901–1910.
Avilés JM, Stokke BG, Moksnes A, Røskaft E, Møller AP. 2007. Environmental conditions influence egg color of reed warblers Acrocephalus scirpaceus and their parasite, the common cuckoo Cuculus canorus. Behav Ecol Sociobiol, 61:475–485.
Avilés JM, Vikan JR, Fossøy F, Antonov A, Moksnes A, Røskaft E, Shykoff JA, Møller AP, Jensen H, Prochazka P, Stokke BG. 2011. The common cuckoo Cuculus canorus is not locally adapted to its reed warbler Acrocephalus scirpaceus host. J Evol Biol. 24:314–325.
Avilés JM, Vikan JR, Fossøy F, Antonov A, Moksnes A, Røskaft E, Shykoff JA, Møller AP, Stokke BG. 2012. Egg phenotype matching by cuckoos in relation to discrimination by hosts and climatic conditions. Proc R Soc Lond B, 279:1967–1976.
Antonov A, Stokke BG, Vikan JR, Fossøy F, Ranke PS, Røskaft E, Moksnes A, Møller AP, Shykoff JA. 2010. Egg phenotype differentiation in sympatric cuckoo Cuculus canorus gentes. J Evol Biol, 23:1170–1182.
Briskie JV, Sealy SG, Hobson KA. 1992. Behavioral defenses against avian brood parasitism in sympatric and allopatric host populations. Evolution, 46:334–340.
Brooke MD, Davies NB, Noble DG. 1998. Rapid decline of host defences in response to reduced cuckoo parasitism: Behavioural flexibility of reed warblers in a changing world. Proc R Soc Lond B, 265:1277–1282.
Cox WA, Thompson FR 3rd, Root B, Faaborg J. 2012. Declining brown-headed cowbird (Molothrus ater) populations are associated with landscape-specific reductions in brood parasitism and increases in songbird productivity. PLoS ONE, 7(10):e47591.
Cruz A, Wiley JW. 1989. The decline of an adaptation in the absence of a presumed selection pressure. Evolution, 43:55–62.
Davies NB, Brooke MD. 1989. An experimental study of co-evolution between the cuckoo, Cuculus canorus, and its hosts. 1. Host egg discrimination. J Anim Ecol, 58:207–224.
De Neve L, Soler JJ, Soler M, Perez-Contreras T. 2004. Differential maternal investment counteracts for late breeding in magpies Pica pica: an experimental study. J Avian Biol, 35:237–245.
Gomulkiewicz R, Drown DM, Dybdahl MF, Godsoe W, Nuismer SL, Pepin KM, Ridenhour BJ, Smith CI, Yoder JB. 2007. Dos and don’ts of testing the geographic mosaic theory of coevolution. Heredity, 98:249–258.
Gomulkiewicz R, Thompson JN, Holt RD, Nuismer SL, Hochberg ME. 2000. Hot spots, cold spots, and the geographic mosaic theory of coevolution. Am Nat, 156:156–174.
Grim T. 2002. Why is mimicry in cuckoo eggs sometimes so poor? J Avian Biol, 33:302–305.
Hargitai R, Moskát C, Bán M, Gil D, López-Rull I, Solymos E, 2010. Eggshell characteristics and yolk composition in the common cuckoo Cuculus canorus: Are they adapted to brood parasitism? J Avian Biol, 41:1–9.
Hauber ME. 2001. Site selection and repeatability in Brown-Headed Cowbird (Molothrus ater) parasitism of Eastern Phoebe (Sayornis phoebe) nests. Can J Zool, 79:1518–1523.
Hauber ME, Strausberger BM, Feldheim KA, Lock J, Cassey P. 2012. Indirect estimates of breeding and natal philopatry in an obligate avian brood parasite. J Ornithol, 153:467–475.
Hochberg ME, van Baalen M. 1998. Antagonistic coevolution over productivity gradients. Am Nat, 152:620–634.
Honza M, Prochazka P, Pozgayova M. 2012. Within- and between-season repeatability of eggshell colouration in the great reed warbler Acrocephalus arundinaceus. J Avian Biol, 43:91–96.
Hoover JP, Yasukawa K, Hauber ME. 2006. Spatially and temporally structured avian brood parasitism affects the fitness benefits of hosts’ rejection strategies. Anim Behav, 72:881–890.
Jensen WE, Cully JF. 2005. Geographic variation in brown-headed cowbird (Molothrus ater) parasitism on Dickcissels (Spiza americana) in great plains tallgrass prairie. Auk, 122:648–660.
Jewell KJ, Arcese P. 2008. Consequences of parasite invasion and land use on the spatial dynamics of host populations. J Appl Ecol, 45:1180–1188.
Lahti DC. 2005. Evolution of bird eggs in the absence of cuckoo parasitism. Proc Natl Acad Sci USA, 102:18057–18062.
Langmore NE, Feeney WE, Crowe-Riddell J, Luan H, Louwrens KM, Cockburn A. 2012. Learned recognition of brood parasitic cuckoos in the superb fairy-wren Malurus cyaneus. Behav Ecol, 23:798–805.
Lindholm AK. 1999. Brood parasitism by the cuckoo on patchy reed warbler populations in Britain. J Anim Ecol, 68:293–309.
Lindholm AK. 2000. Tests of phenotypic plasticity in reed warbler defences against cuckoo parasitism. Behaviour, 137:43–60.
Lindholm AK, Thomas RJ. 2000. Differences between populations of reed warblers in defences against brood parasitism. Behaviour, 137:25–42.
Martín-Gálvez D, Soler JJ, Martínez JG, Krupa AP, Richard M, Soler M, Møller AP, Burke T. 2006. Genetic basis for recognition of foreign eggs in the host of a brood parasite. J Evol Biol, 19:543–550.
Martín-Gálvez D, Soler JJ, Martínez JG, Krupa AP, Soler M, Burke T. 2007. Cuckoo parasitism and productivity in different magpie subpopulations predict frequencies of the 457bp allele: A mosaic of coevolution at a small geographic scale. Evolution, 61:2340–2348.
Moksnes A, Røskaft E. 1995. Egg-morphs and host preference in the common cuckoo (Cuculus canorus): an analysis of cuckoo and host eggs from European museum collections. J Zool Lond, 236:625–648.
Moksnes A, Røskaft E, Braa AT. 1991. Rejection behavior by common cuckoo hosts towards artificial brood parasite eggs. Auk, 108:348–354.
Møller AP, Antonov A, Stokke BG, Fossøy F, Moksnes A, Røskaft E, Takasu F. 2011a. Isolation by time and habitat and coexistence of distinct host races of the common cuckoo. J Evol Biol, 24:676–684.
Møller AP, Garamszegi LZ, Peralta-Sánchez JM, Soler JJ. 2011b. Migratory divides and their consequences for dispersal, population size and parasite-host interactions. J Evol Biol, 24:1744–1755.
Møller AP, Saino N, Adamik P, Ambrosini R, Antonov A, Campobello D, Stokke BG, Fossøy F, Lehikoinen E, Martín-Vivaldi M, Moksnes A, Moskat C, Røskaft E, Rubolini D, Schulze-Hagen K, Soler M, Shykoff JA. 2011c. Rapid change in host use of the common cuckoo Cuculus canorus linked to climate change. Proc R Soc Lond B, 278:733–738.
Møller AP, Soler JJ, Martín Vivaldi M. 2010. Spatial heterogeneity in distribution and ecology of Western Palearctic birds. Ecology, 91:2769–2782.
Moreno J, Osorno JL. 2003. Avian egg colour and sexual selection: does eggshell pigmentation reflect female condition and genetic quality? Ecol Lett, 6:803–806.
Moskát C, Hansson B, Barabas L, Bartol I, Karcza Z. 2008. Common cuckoo Cuculus canorus parasitism, antiparasite defence and gene flow in closely located populations of great reed warblers Acrocephalus arundinaceus. J Avian Biol, 39:663–671.
Moskát C, Szentpeteri J, Barta Z. 2002. Adaptations by great reed warblers to brood parasitism: A comparison of populations in sympatry and allopatry with the common cuckoo. Behaviour, 139:1313–1329.
Nakamura H. 1990. Brood parasitism by the cuckoo Cuculus canorus in Japan and the start of new parasitism on the azure-winged magpie Cyanopica cyana. Japn J Ornithol, 39:1–18.
Nakamura H, Kubota S, Suzuki R. 1998. Coevolution between the common cuckoo and its major hosts in Japan. In: Rothstein SI, Robinson SK (eds) Parasitic Birds and Their Hosts: Studies in Coevolution. Oxford University Press, New York, pp 94–112.
Norton DA, Carpenter MA. 1998. Mistletoes as parasites: host specificity and speciation. Trends Ecol Evol, 13:101–105.
Parejo D, Avilés JM. 2007. Do avian brood parasites eavesdrop on heterospecific sexual signals revealing host quality? A review of the evidence. Anim Cogn, 10:81–88.
Robert M, Sorci G. 1999. Rapid increase of host defence against brood parasites in a recently parasitized area: The case of village weavers in Hispaniola. Proc R Soc Lond B, 266:941–946.
Rothstein SI. 1990. A model system for coevolution: avian brood parasitism. Ann Rev Ecol Evol Syst, 21:481–508.
Soler JJ, Avilés JM, Moller AP, Moreno J. 2012. Attractive blue-green egg coloration and cuckoo-host coevolution. Biol J Linn Soc, 106:154–168
Soler JJ, Martín-Gálvez D, Martínez JG, Soler M, Canestrari D, Abad-Gomez JM, Møller AP. 2011. Evolution of tolerance by magpies to brood parasitism by great spotted cuckoos. Proc R Soc Lond B, 278:2047–2052.
Soler JJ, Martín-Vivaldi M, Møller AP. 2009. Geographic distribution of suitable hosts explains the evolution of specialized gentes in the European cuckoo Cuculus canorus. BMC Evol Biol, 9:88.
Soler JJ, Martínez JG, Soler M, Møller AP. 1999a. Host sexual selection and cuckoo parasitism: An analysis of nest size in sympatric and allopatric magpie Pica pica populations parasitised by the great spotted cuckoo Clamator glandarius. Proc R Soc Lond B, 266:1765–1771.
Soler JJ, Martínez JG, Soler M, Møller AP. 1999b. Genetic and geographic variation in rejection behavior of cuckoo eggs by European magpie populations: An experimental test of rejecter-gene flow. Evolution, 53:947–956.
Soler JJ, Martínez JG, Soler M, Møller AP. 2001a. Host life-history and brood parasitism: An analysis of sympatric and allopatric magpie populations parasitized by the great spotted cuckoo Clamator glandarius. Ecology, 82:1621–1631.
Soler JJ, Martínez JG, Soler M, Møller AP. 2001b. Coevolutionary interactions in a host-parasite meta-population. Ecol Lett, 4:470–476.
Soler JJ, Soler M, Møller AP, Martínez JG. 1995. Does the great spotted cuckoo choose magpie hosts according to their parenting ability? Behav Ecol Sociobiol, 36:201–206.
Soler M. 1990. Relationships between the great spotted cuckoo Clamator glandarius and its corvid hosts in a recently colonized area. Ornis Scand, 21:212–223.
Soler M, Martín-Vivaldi M, Fernández-Morante J. 2012. Conditional response by hosts to parasitic eggs: The extreme case of the rufous-tailed scrub robin. Anim Behav, 84:421–426.
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, Soler JJ, Martínez JG, Møller AP. 1994. Micro-evolutionary change in host response to a brood parasite. Behav Ecol Sociobiol, 35:295–301.
Stokke BG, Hafstad I, Rudolfsen G, Bargain B, Beier J, Campàs DB, Dyrcz A, Honza M, Leisler B, Pap PL, Patapavicius R, Procházka P, Schulze-Hagen K, Thomas R, Moksnes A, Møller AP, Røskaft E, Soler M. 2007. Host density predicts presence of cuckoo parasitism in reed warblers. Oikos, 116:913–922.
Stokke BG, Hafstad I, Rudolfsen G, Moksnes A, Møller AP, Røskaft E, Soler M. 2008. Predictors of resistance to brood parasitism within and among reed warbler populations. Behav Ecol, 19:612–620.
Strausberger BM. 2001. The relationship of habitat and spatial distribution of nests with brown-headed cowbird parasitism of Red-winged Blackbirds. Wilson Bull, 113:129–133.
Takasu F. 2003. Co-evolutionary dynamics of egg appearance in avian brood parasitism. Evol Ecol Res, 5:345–362.
Tewksbury JJ, Garner L, Garner S, Lloyd JD, Saab V, Martin TE. 2006. Tests of landscape influence: Nest predation and brood parasitism in fragmented ecosystems. Ecology, 87:759–768.
Thompson FR. 1994. Temporal and spatial patterns of breeding Brown-Headed Cowbirds in the Midwestern United-States. Auk, 111:979–990.
Thompson JN. 1994. The Coevolutionary Process. University of Chicago Press, Chicago.
Thompson JN. 2005. The Geographic Mosaic of Coevolution, The University of Chicago Press, Chicago.
Underwood TJ, Sealy SG, McLaren CM. 2004. Eastern Wood-Pewees as Brown-headed Cowbird hosts: accepters but infrequently parasitized. J Field Ornithol, 75:165–171.
Vikan JR, Fossøy F, Huhta E, Moksnes A, Røskaft E, Stokke BG. 2011. Outcomes of brood paraite-host interactions mediated by egg matching: Common cuckoos Cuculus canorus versus Fringilla finches. PLoS ONE, 6(4):e19288.
Zuñiga JM, Redondo T. 1992. No evidence for variable duration of sympatry between the great spotted cuckoo and its magpie host. Nature, 359:410–411.
Similar articles

Copyright by Chinese Birds