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Tuesday, 13 May 2014

Egg colour variation and egg rejection in response to Cuckoo parasitism. Yang et al Evolution and Ecology 7 May 2014

Egg color variation, but not egg rejection behavior, changes in a cuckoo host breeding in the absence of brood parasitism

Canchao Yang 1, Yang Liu 2, Lijin Zeng 3 and Wei Liang 1*

Author Information
1- Ministry of Education Key Laboratory for Tropical Animal and Plant Ecology, College of Life Sciences, Hainan Normal University, Haikou, China
2- State Key Laboratory of Biocontrol and School of Life Sciences, Sun Yat-sen University, Guangzhou, China
3- Department of Biology, University of California, Riverside, California, USA
* Correspondence 

Wei Liang, Ministry of Education Key Laboratory for Tropical Animal and Plant Ecology, College of Life Sciences, Hainan Normal University, Haikou 571158, China. Tel: +86 898 65883521; Fax: +86 898 65818360; E-mail:

Article first published online: 7 MAY 2014


DOI: 10.1002/ece3.1096

Original Research - Online Open Access article

© 2014 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.


Interactions between parasitic cuckoos and their songbird hosts form a classical reciprocal “arms race,” and are an excellent model for understanding the process of coevolution. Changes in host egg coloration via the evolution of interclutch variation in egg color or intraclutch consistency in egg color are hypothesized counter adaptations that facilitate egg recognition and thus limit brood parasitism. Whether these antiparasitism strategies are maintained when the selective pressure of parasitism is relaxed remains debated. However, introduced species provide unique opportunities for testing the direction and extent of natural selection on phenotypic trait maintenance and variation. Here, we investigated egg rejection behavior and egg color polymorphism in the red-billed leiothrix (Leiothrix lutea), a common cuckoo (Cuculus canorus) host, in a population introduced to Hawaii 100 years ago (breeding without cuckoos) and a native population in China (breeding with cuckoos). We found that egg rejection ability was equally strong in both the native and the introduced populations, but levels of interclutch variation and intraclutch consistency in egg color in the native population were higher than in the introduced population. This suggests that egg rejection behavior in hosts can be maintained in the absence of brood parasitism and that egg appearance is maintained by natural selection as a counter adaptation to brood parasitism. This study provides rare evidence that host antiparasitism strategies can change under parasite-relaxed conditions and reduced selection pressure.

Study species and study areas

The red-billed leiothrix (Leiothrichidae) is a medium-sized, green-and-yellow babbler with a conspicuous bright red bill. It is a common resident species native to the Himalayas, Myanmar, southern China, and Vietnam where it is found in a wide variety of habitats, including broadleaf evergreen, pine and mixed forests, forest edges, secondary growth, and varied scrub, from sea level to 4000 m a.s.l. It was recorded as one of the normal hosts of the common cuckoo in India (Baker 1942) and builds open-cup nests in branches in dense vegetation and lays polymorphic eggs that vary in color from white to bluish-green with blood-red marking patterns (Fig. 1). 

Figure 1
Eggs and nests of the red-billed leiothrix (Leiothrix lutea). Photograph by C. Yang.

Egg rejection ability and egg color variation in songbirds species are considered to be defensive strategies that evolved to limit cuckoo parasitism and, hence, are traits believed to be under strong selection. Here, we have shown that internest variation in the chroma and brilliance of egg background color and intranest variation in the UV component of hue and the brilliance of ground-color and markings are lower in populations of red-billed leiothrix when cuckoos are present. To our knowledge, this is the one of the first examples that host antiparasitism strategies of hosts can change under a parasite-relaxed conditions and reduced selection pressure.

The maintenance of egg rejection ability is independent of cuckoos
Our results indicated no difference in egg recognition or rejection ability between the introduced and native populations of leiothrix because almost all foreign eggs were rejected on the first day of the experiment by both groups. Similar results were found by Lahti (2006) in an experiment conducted on two introduced populations of village weaverbird. These results indicate that hosts' egg recognition ability in hosts decays very slowly and can be maintained for a long time following a species' escape from brood parasitism. Rothstein (2001) also found that host populations descended from lineages likely to have been parasitized, but not parasitized currently, continue to eject nearly 100% of nonmimetic eggs. The persistence of this adaptive behavior under relaxed selection pressure may indicate that it is not costly to maintain (Kuehn et al. 2014). In line with host-parasite systems, previous studies showed that antipredation behavior requires several hundreds to even thousands of years to disappear in island populations after a relaxation in predation pressure (Magurran et al. 1992; Blumstein et al. 2000).

However, the acquisition of egg recognition can occur quite rapidly. For example, after their initial exposure to parasitism by cuckoos, the egg rejection rates in azure-winged magpies (Cyanopica cyana) increased from 0% to 30–60% in just 20 years (Nakamura 1990; Nakamura et al. 1998). Similarly, the egg rejection rate of the magpies (Pica pica) to eggs of the great spotted cuckoo (Clamator glandarius) increased from 0% to 10% in just 10 years (Soler et al. 1994). This rate of behavioral change is too rapid to be a consequence of genetic change (Davies and Welbergen 2009) and is more likely to be the result of transmission via social learning (Soler 2011); a suggestion that was confirmed by the mobbing behavior of hosts (Davies and Welbergen 2009). The acquisition of egg recognition may occur more rapidly than its loss because it occurs under strong, directional selection pressure on the particular hosts. In the absence of brood parasites, however, selection pressure is not reversed but simply released, such that the trait continues to evolve under neutral selection and only a new selective pressure can accelerate its rate of change in that particular trait. For example, strong egg rejection rates in hosts result in rejection errors, and subsequently, rejection of their own eggs and natural selection will favor reduced egg rejection behavior in hosts. While social learning may influence the uptake of egg rejection behavior, our finding of persistent egg rejection in populations free from brood parasites supports the idea that egg recognition behavior in leiothrix has a strong genetic basis.

Differences in egg color between native and introduced host populations could be the result of relaxed selection of cuckoo parasitism
We found increased interclutch variation and intraclutch consistency, but no change in the intraclutch consistency of egg background color and markings in the native population compared with the introduced populations. However, the RGB component of the hue disparity of egg markings between nests followed the opposite pattern, possibly because egg markings are not a critical cue in egg recognition. For example, a field experiment revealed that leiothrix uses egg ground-color rather than markings to recognize their own eggs and discriminate alien eggs (C. Yang, Y. Liu, and W. Liang, unpubl. data).

It has been proposed that random mechanisms such as gradual genetic drift and founder effects can result in phenotypic shifts in recently colonized island populations (Lande 1976). However, it is unlikely that such random processes alone caused the observed differences in eggs detected here (Fig. 3 and 4) because (1) current populations across the Hawaiian archipelago were introduced multiple times between 1911 and 1937 (Fisher and Baldwin 1947), and the overall population size here is estimated to be tens of thousands in Hawaii (Male et al. 1998) and regarded stable (Ralph et al. 1998); and (2) founder effects could not be the only process driving changes in egg color in the introduced population. If founder effects played a deterministic role regarding differences in egg color between introduced and native populations, the color spectrum was more disperse in the studied population than which in native populations, whereas the effect of founder effect would be more dispersed in the native population. Our results do not support this and we instead posit that release from cuckoo parasitism-driven selection pressure plays a role in driving shifts in egg color.

Hypotheses explaining intra- and interclutch variation in egg color polymorphism have spawned a cottage industry of empirical testing; however, the experimental evidence supporting this hypothesis has been mixed (Stokke et al. 1999, 2002; Karcza et al. 2003; Avilés et al. 2004). For example, Yang et al. (2010) revealed that brood parasitism from the common cuckoo exerts a disruptive selection on its host, the ashy-throated parrotbill (Paradoxornis alphonsianus), driving coevolution of polymorphic egg color in these two species. Empirical studies comparing host rejection behavior and egg color variation between native and introduced populations, with and without cuckoo parasitism, have rarely been reported before. One impressive and systematic study from Lahti (2005) showed that both the intraclutch consistency and interclutch variation in egg appearance of the village weaverbird decreased in two introduced populations which had existed without egg-mimicking brood parasites for more than 100 and 200 years, in comparison with the native population. Interestingly, in that study, the difference in interclutch variation between the source and the introduced populations was only significant when comparing the older introduced population (i.e., 200 years), although a trend in the general direction was observed in the younger introduced population (Lahti 2005). Here, we report that significant changes in interclutch variation and intraclutch consistency in egg color between native and introduced populations can occur on a timescale of approximately <100 years. These results further support the hypothesis that polymorphic egg appearance is a strongly selected trait under brood parasitism pressure of brood parasitism.

In comparison with egg rejection behavior, changes in egg color variation apparently evolve rapidly (e.g., in approximately 100 years in the present study). This disparity may be a consequence of the fact that egg appearance is also under concurrent selection to optimize factors other than minimizing brood parasitism, such as maximizing solar radiation and minimizing predation (Moreno and Osorno 2003). Egg coloration is likely to be a consequence of local adaptation to specific environments (Mathys and Lockwood 2011) and may be correlated with female's genetic quality (Moreno and Osorno 2003), which interact with each other when multiple sources of selection (natural and sexual) coexist. Thus, geographic differences between native and introduced populations are likely to have a far greater influence on egg appearance than on egg rejection behavior. As the investment of eggshell pigments is costly (Moreno and Osorno 2003; López-Rull et al. 2008; Sanz and García-Navas 2009), subsequent selection after removal of brood parasitism may favor hosts to reduce this unnecessary expenditures, resulting in decreased population variation in egg coloration. However, it remains unclear to what extent biotic and abiotic constraints shape egg color variation and egg rejection behavior. Combined, we provide rare empirical evidence that egg traits functioned as cues for recognizing alien eggs by hosts changed due to relaxed selection, as opposed to egg rejection ability per se. Since both egg coloration and recognition have a heritable basis and are probably driven by both natural and sexual selection (Moreno and Osorno 2003), an investigation into the genetic architecture of complex traits and their changes under context-dependent selection and other evolutionary processes is needed.

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