Sex roles in egg recognition and egg polymorphism in avian brood parasitism

Behavioral Ecology doi:10.1093/beheco/arr203 Advance Access publication 1 December 2011 Original Article Sex roles in egg recognition and egg polymorphism in avian brood parasitism Wei Liang,a Canchao Yang,a,b Anton Antonov,c Frode Fossøy,c Bård G. Stokke,c Arne Moksnes,c Eivin Røskaft,c Jacqui A. Shykoff,d Anders P. Møller,d and Fugo Takasue a College of Life Sciences, Hainan Normal University, Haikou 571158, P. R. China, bState Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-sen Unviersity, Guangzhou 510275, P. R. China, c Department of Biology, Norwegian University of Science and Technology, Trondheim NO-7491, Norway, dLaboratoire d’Ecologie, Systématique et Evolution, CNRS UMR 8079, Université Paris-Sud, Bâtiment 362, F-91405 Orsay Cedex, France, and eDepartment of Information and Computer Sciences, Nara Women’s University, Kita-Uoya Nishimachi, Nara 630–8506, Japan Avian brood parasites impose strong selection on their hosts leading to the evolution of antiparasite defenses like egg recognition and rejection. Discordance and template-based cognitive mechanisms may form the base for egg recognition by hosts. For discordance, hosts recognize eggs that constitute the minority in a clutch as alien, whereas in template-based recognition, hosts recognize eggs as alien when they do not match a template that can be innate or learnt. Template-based recognition by learning can be compromised in host species with polymorphic egg color like Paradoxornis parrotbills, hosts of the common cuckoo Cuculus canorus, because a male that learns an egg color in his first breeding attempt can subsequently mate with females having different colors and therefore reject his own eggs. We present a simple conceptual model to understand how an asymmetry in sex roles of care for eggs and egg polymorphism influence the evolution of egg recognition by hosts. We derive host reproductive success in the presence of variation in egg phenotype for both host and parasite. Our model shows that male recognition by learning is disadvantageous unless the host has monomorphic eggs. We suggest that interclutch variation in egg phenotype is the key to understanding the evolution of egg recognition and the sex involved. Key words: avian brood parasitism, discordance, egg polymorphism, egg recognition, learning and imprinting, template-based. [Behav Ecol 23:397–402 (2012)] INTRODUCTION vian brood parasites impose strong selection pressure on their hosts leading to the evolution of antiparasite defenses (Rothstein 1990; Davies 2000). Many hosts of brood parasites have evolved the ability to recognize and reject parasite eggs (Rothstein 1975; Davies and Brooke 1989a, 1989b; Moksnes et al. 1991) and some hosts use multiple visual cues to reject foreign eggs (Spottiswoode and Stevens 2010). However, it remains an open question how the hosts recognize and pinpoint a parasitic egg in the clutch. 2 major cognitive mechanisms have been proposed; recognition by discordance and template-based recognition (Rothstein 1974, 1978; Lotem et al. 1992; Moksnes and Røskaft 1992; Lotem 1993; Hauber et al. 2006; Moskát et al. 2010). In recognition by discordance, hosts recognize eggs as alien whose phenotype is a minority in the clutch (Rothstein 1974). Discordance would be the simplest cognitive mechanism, and it logically works as an antiparasite defense if parasitism rate is low and if multiple parasitism is rare. Recognition by discordance has been thought unlikely (Rothstein 1974), but recent experimental studies suggest this possibility for some hosts (Marchetti 2000; Moskát et al. 2010). A Address correspondence to Fugo Takasu. E-mail: -wu. ac.jp. Wei Liang and Canchao Yang contributed equally to this work. Received 15 March 2011; revised 28 August 2011; accepted 5 October 2011.
The Author 2011. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions, please e-mail: In template-based recognition, on the other hand, hosts know the phenotype of their own eggs and any egg that does not match a ‘‘template’’ is considered alien (Rothstein 1974, 1978). The template can be either innate or learnt by an imprinting-like process (Rothstein 1974, 1978; Hauber and Sherman 2001; Hauber et al. 2001). It has been demonstrated that some hosts use a learnt template; they learn and imprint on eggs of their first clutch and reject eggs that do not match the learnt template in subsequent breeding attempts (Victoria 1972; Rothstein 1978; Lotem et al. 1995). Recognition by learning is effective if the template is formed correctly in the sense that the host has imprinted on its own eggs. Although some studies have shown that there is no age-specific difference in recognition ability, suggesting that no learning is involved in egg recognition in some host species (Marchetti 2000; Amundsen et al. 2002; Stokke et al. 2004), learning can be an important component of host defenses against parasitism in other hosts (Rothstein 1974; Strausberger and Rothstein 2009; Moskát et al. 2010; Shizuka and Lyon 2010). Recognition by learning logically works for females that produce eggs and hence should be able to correctly imprint on their own eggs immediately after laying. However, it does not necessarily work for males that often have fewer opportunities to observe eggs in their nest. Asymmetry in sex roles in the producing and caring for eggs is thus likely to influence the evolution of recognition by learning by restricting or even precluding the male’s learning ability, whereas recognition by discordance is not affected by such an asymmetry. It generally remains unclear on which sex is responsible for the egg recognition and rejection of parasitic eggs (Davies Behavioral Ecology 398 and Brooke 1988; Sealy and Neudorf 1995; Lee et al. 2005; Honza et al. 2007). However, it has been demonstrated that in host species where only the females incubate, only females recognize and reject unlike eggs, whereas both the sexes reject in species where both sexes incubate (Soler et al. 2002; Požgayová et al. 2009). This finding is consistent with the idea that recognition by learning both by females and males works as an effective defense mechanism against parasitism. Recognition by learning for males, however, can be compromised if there is polymorphism in egg phenotype. Paradoxornis parrotbills, hosts of the common cuckoo Cuculus canorus, and several other host species show a clear polymorphism in egg color. For instance, in the vinous-throated parrotbill P. webbianus in South Korea, each female produces either blue or white eggs (Kim et al. 1995; Lee and Yoo 2004; Lee et al. 2005). It is also known that both the sexes take part in incubation, in this species (Lee et al. 2005; Jiang et al. 2009). The ashy-throated parrotbill P. alphonsianus in southern China shows 3 distinct phenotypes, producing white, blue, or pale blue eggs (Yang et al. 2010). Thes (...truncated)