Evolution of defences against cuckoo Emphasis Ty

Authors: Johan Reinert Vikan Bård Gunnar Stokke Jarkko Rutila Esa Huhta Arne Moksnes Eivin Røskaft

Publish Date: 2010/02/18

Volume: 24, Issue: 5, Pages: 1141-1157

PDF Link

Abstract

The brood parasitic common cuckoo Cuculus canorus has a history of coevolution that involves numerous passerine hosts but today only a subset is known to be regularly parasitised in any area In some hosts there is significant variation in the occurrence of parasitism between populations but still individuals in nonparasitised populations show strong antiparasite defences In the present study we compared the strength of egg rejection of four distant Fennoscandian brambling Fringilla montifringilla populations experiencing different levels of cuckoo parasitism 0–6 Egg rejection ability was in general very well developed and we did not find any population differences in the relationship between egg rejection probability and similarity between host and experimental parasitic eggs Furthermore bramblings very rarely made errors in rejection indicating that selection against rejection behaviour is likely to be very weak The bramblingcuckoo system therefore differs from other well studied systems which are characterised by pronounced spatial and temporal variation in the host’s level of defence This result is unlikely to reflect independent replication of the same evolutionary trajectory because the weak breeding site tenacity of bramblings should result in an extreme amount of gene flow within the distribution area and thus strongly impede localised responses to selection Instead lack of geographic variation has more likely arisen because bramblings respond to selection as one evolutionary unit and because the average parasitism pressures have been high enough in the past to cause regional fixation of rejection alleles and evolution of clutch characteristics that facilitate cost free egg recognitionThe common cuckoo Cuculus canorus hereafter cuckoo and its passerine hosts experience a diverse set of interactions regarding the existence and sophistication of coevolved traits Rothstein and Robinson 1998 Davies 2000 An intriguing trend uncovered by broad community level investigations is that suitable but nonparasitised hosts tend to discriminate more strongly against parasitic eggs than do regularly parasitised hosts Davies and Brooke 1989b Moksnes et al 1991 This suggests that the subset of hosts involved in interactions with the cuckoo changes through time and that local evolution of host defence is a potentially important factor in this process by promoting host switches and/or local extinction of specialist parasite tribes gentes Davies and Brooke 1998 Nakamura et al 1998 Nuismer and Thompson 2006A limitation in most of these studies is that they cover geographically restricted areas and short time spans Rothstein and Robinson 1998 This is problematic because the state of interacting populations can be influenced by a multitude of ecological historical and geographical factors Thompson 2005 For example selection pressures acting upon host and parasites for interaction traits may vary significantly in intensity between areas according to the prevailing ecological settings eg Brodie et al 2002 Siepielski and Benkman 2004 Toju and Sota 2006 MartínGálvez et al 2007 Stokke et al 2007a Parchman and Benkman 2008 Moreover the interaction in one locality may be influenced by the interaction in others through gene flow eg Dybdahl and Lively 1996 Nuismer et al 1999 Soler et al 1999 Gomulkiewicz et al 2000 Røskaft et al 2006 Moskát et al 2008b Consequently inferring the processes behind local trait patterns requires extensive geographical sampling and consideration of the spatial dynamics of the interacting parties Thompson 2005The potential importance of spatial dynamics in hostparasite coevolution has had a growing influence on empirical studies of brood parasitehost interactions in the last decade Stokke et al 2005 So far however only a small and biased subset of hosts has been thoroughly examined For example most of the hosts examined show low defence levels in populations allopatric with the cuckoo eg Stokke et al 2008 whereas population comparisons are scarce for hosts that show high defence levels in nonparasitised populations In general investigation of a more diverse set of systems would add useful bricks to the edifice of our understanding of cuckoohost coevolution and its diverse outcomesThe present study concerns the interaction between bramblings Fringilla montifringilla and cuckoos in Fennoscandia Among potential cuckoo hosts in Europe the brambling represents an extreme case with regard to population genetic structure It is a northern boreal species which employs an opportunistic breeding strategy for exploitation of favourable but unpredictable breeding opportunities Hogstad 2000 2005 Lindström et al 2005 It has therefore very low breeding site tenacity Mikkonen 1983 Lindström 1987 Fransson and HallKarlson 2008 and ringing recoveries indicate that bramblings may breed at sites up to 600 km apart in different years Lindström 1987 This pervasive aspect of brambling ecology should strongly impede any localised responses to selection eg Hendry et al 2001 Lenormand 2002 Nash et al 2008 Parchman and Benkman 2008 Accordingly in spite of having a wide breeding distribution implying that it has been subject to a vast array of environmental selection pressures no subspecies are recognised Cramp and Perrins 1994 Hogstad and Väisänen 1997 The brambling has long been known as a cuckoo host in northern Finland and northwestern Russia where there are several accounts of cuckoo eggs that mimic brambling eggs Montell 1917 Wasenius 1936 Baker 1942 Malchevsky 1987 Numerov 2003 whereas records from other parts of Fennoscandia are sparse Nevertheless in Central Norway where parasitism has never been recorded bramblings were observed to reject 90 of artificial cuckoo eggs both nonmimetic eggs and eggs painted to resemble brambling eggs which makes it a candidate example of an expired cuckoohost interaction as suggested by Braa et al 1992 The aim of the present study was to examine geographical variation in brambling defences to cuckoo parasitism egg rejection and aggression to cuckoo dummies including both parasitised and nonparasitised populations and to discuss evolution of these defences in light of the distribution of current/historical selection and the spatial dynamics of the bramblingThe data material was collected during the breeding seasons 2003–2008 Tana in June–July 2003–2004 Kittilä in May–June 2005–2008 Tydal in June–July 2005–2007 and Ammarnäs in June–July 2008 Most nests were visited daily during egg laying and each egg in a clutch was marked with waterproof ink in sequence as laid If necessary laying dates were estimated from floating tests of the eggs Hays and Lecroy 1971 and if available hatching datesPlate indicating the range of variation of brambling clutches rows 1–3 Each egg represents a different clutch N = 15 Bottom row provides examples of cuckoo eggs found in brambling nests in Kittilä The eggs are not scaled according to relative sizes

Keywords: