Exploring plasticity in the wild: laying date–temperature reaction norms in the common gull Larus canus

Jon E. Brommer 2 3 Kalev Rattiste 1 2 Alastair J. Wilson 0 2 0 Ashworth Laboratories, Institute of Evolutionary Biology, School of Biological Sciences, The University of Edinburgh , The King's Buildings, West Mains Road, Edinburgh EH9 3JT , UK 1 Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences , 181 Riia Street, 51014 Tartu , Estonia 2 One contribution of 18 to a Special Issue 'Evolutionary dynamics of wild populations' 3 Bird Ecology Unit, Department of Biological and Environmental Sciences, University of Helsinki , PO Box 65, (Viikinkaari 1), 00014 Helsinki , Finland Exploration of causal components of plasticity is important for insight into evolutionary dynamics and an organism's ability to respond to climate change. Among individuals, variation in plasticity can be due to genotype-environment interaction (G!E) or a result from environmental effects associated with an individual. We investigated plasticity for laying date in the common gulls Larus canus, using data collected in Estonia during 37 years (nZ11 624 records on 2262 females, with 472 relatives). We used a sliding window approach to find the period in spring during which mean temperature best explained the annual mean laying date. Then, considering the spring temperature as a quantitative description of the environment, we used pedigree information and a random regression animal model to determine the variation in plasticity for the laying date-temperature relationship. We found that individuals differ in the plasticity of laying date (such that there is increased variation among individuals for the laying date in warmer springs), and that approximately 11% of variation in the laying date is heritable, but we found no statistical support for G!E. Plasticity in this species is not constrained by warmer springs. 1. INTRODUCTION Temperature has a profound impact on the seasonal timing of many life-history events in iteroparous organisms, including migration ( Jonzen et al. 2006) and reproduction (Reale et al. 2003; Both et al. 2004; Nussey et al. 2005). Temperatures have increased and are projected to increase in the coming decades (IPCC 2007). In response to this global warming, the phenology of an overwhelming number of animals and plants has changed in the recent decades ( Walther et al. 2002; Parmesan 2006), primarily through the mechanism of phenotypic plasticity ( Walther et al. 2002). However, for a proper understanding of how populations will respond to climate change, we need to understand the mechanisms and limitations of such plasticity. For example, can we expect continued advances in phenology if the climate change continues indefinitely? This question is especially relevant for life-history traits, such as the seasonal timing of reproduction, which are clearly related to individual fitness ( Visser et al. 2004). For example, reduced capacity to adjust laying date to a changing environment has been shown to have population-level consequences in the pied flycatcher Ficedula hypoleuca (Both et al. 2006). Long-term studies where repeated measures are made on individuals across multiple years often reveal * Author for correspondence (). heterogeneity in the individual-specific response to climate, with certain individuals being more plastic in their phenology than others. This variation has been termed I!E (individualenvironment interaction; Nussey et al. 2007). Although each individual is a unique genotype, I!E in itself cannot be interpreted equivalent to genotypeenvironment interaction (G!E), because any environmental effects experienced by an individual during its life will be fully confounded with the effects of its genes. Such individual-specific environmental effects are termed permanent environmental effects in quantitative genetics (Lynch & Walsh 1998). Importantly, longitudinal individual-based data allow studying the consequences of plasticity for an individuals fitness, and the causes of plasticity can be studied under natural environmental conditions (Brommer et al. 2003; Nussey et al. 2007). Of particular interest is whether variation in plasticity has a genetic basis (i.e. due to a genotypeenvironment interaction G!E). If so, then plasticity is heritable, and selection has the potential to maintain, or even increase, the capacity of individuals to adjust their phenology to climatic conditions. For example, the climate change has increased selection on plasticity in Dutch great tits (Parus major) that adjust their laying date in response to temperature ( Nussey et al. 2005). While G!E has been shown in this case ( Nussey et al. 2005), similar plastic responses in collared flycatchers Ficedula albicollis show no heritable variation (Brommer et al. 2005). When springs get warmer, this species phenotypic adjustment of laying date to temperature levels off (plasticity decreases) and continued climate warming is thus predicted to constrain plasticity, possibly to such a degree that it can have population-level consequences. Provided a pedigree is available, I!E can be partitioned into genetic and permanent environmental effects. This can be achieved by comparing plasticity across relatives in the population using a particular form of quantitative genetic analysis based on random regressions ( Meyer & Hill 1997; Meyer 1998; Schaeffer 2004; Nussey et al. 2007). A random regression animal model (RRAM) is an implementation of the concept of infinitedimensional reaction norms (Kirkpatrick & Heckman 1989; Gomulkiewicz & Kirkpatrick 1992; Kirkpatrick et al. 1994) within the context of an animal model. Instead of modelling covariances across separate environments ( Via & Lande 1985), an infinite-dimensional reaction norm allows values for additive genetic and other effects to vary as continuous functions of an environmental covariable. Pedigree information can be used to partition the variance in the parameters describing these functions, and this information can be used to describe the (co)variances across environments (e.g. Meyer & Kirkpatrick 2005). Here, we apply an RRAM approach to explore plasticity using data from a long-term study of laying date in the common gulls (Larus canus) breeding in Estonia. Common gulls are long-lived migratory birds that breed in colonies. Laying early is an important life-history decision, and has been shown to be under consistent directional selection in this population (Rattiste 2006). Because we study a natural population, the environment is not controlled, and hence we consider, as a description of the annual environment, the average temperature during a time window that shows the highest correlation with the annual mean laying date. We then use pedigree information to apply a RRAM framework in which a series of models are compared in order to test whether (i) plasticity in the laying datetemperature relationship occurs, (ii) individuals differ in this relationship, and (iii) variation in plasticity across indi (...truncated)