Sources of egg-size variation in house wrens (Troglodytes aedon): Ontogenetic and environmental components

ABSTRACT.-Evolutionary theory predicts that heritability of fitness-related traits should be low. Egg size in birds is a fitness-related trait, but exhibits high heritability. One possible explanation for the apparent failure of natural selection to exhaust variability is that variation in egg size is mediated by female condition. In this study, we estimated repeatability of egg size within and between successive clutches in a wild, double-brooded population of House Wrens (Troglodytes aedon) in central Illinois, and examined the relationship of egg size with female size and condition. Repeatability of egg volume and mass in individual birds was high within years and between successive years (>0.77), suggesting a substantial heritable component to variation in egg size. However, egg mass was also significantly correlated with female condition. We suggest that the high repeatability values largely reflect permanent but nongenetic (ontogenetic) variation in egg size among females, which is reflected in the positive correlation of egg size with female condition. If variation in egg size is attributable to a combination of nonheritable, ontogenetic variation and variation due to current environmental conditions among females, then selection may not produce an evolutionary response in egg size. Received 1 May 2000, accepted 15 April 2002.

RESUMEN.-La teoria evolutiva predice que la heredabilidad de los caracteres relacionados con la adecuacion biologica debe ser baja. El tamano del huevo de las aves es un caracter relacionado con la adecuacion, pero presenta alta heredabilidad. Una posible explicacion para la aparente incapacidad de la seleccion natural de agotar la variabilidad, es que la variacion en el tamano del huevo sea med iada por la condicion de las hembras. En este estudio, estimamos que tan repetible es el volumen del huevo dentro y entre nidadas sucesivas en una poblacion de Troglodytes aedon con dos nidadas anuales en el centro de Illinois. Tambien exam inamos la relacion entre el tamano del huevo y el tamano y la condicion de las hembras. El volumen y la masa del huevo en aves individuales fue altamente repetible dentro de anos y entre anos consecutivos (>0.77), lo que sugiere que la variacion en el tamano del huevo tiene un componente heredable importante. Sin embargo, la masa del huevo tambien estuvo correlacionada significativamente con la condicion de las hembras. Sugerimos que la alta repetibilidad de los valores refleja en gran medida variacion permanente pero no genetica (ontogenetica) en el tamano del huevo entre hembras, lo cual se refleja en la correlacion positiva entre el tamano del huevo y la condicion de las hembras. Si la variacion en el tamano del huevo puede atribuirse a una combinacion de variacion ontogenetica no heredable con variacion debida a las condiciones ambientales del momento entre las hembras, la seleccion no podria producir una respuesta evolutiva en el tamano del huevo.

EGG SIZE is an important maternal effect in birds, affecting posthatching growth and development of nestlings (Williams 1994, Bernardo 1996, Price 1998, Merila and Sheldon 2001). Within the past decade, studies on species that span the altricial-precocial spectrum of nestling development have demonstrated experimentally that egg mass, independent of female ability to incubate eggs or to raise a brood, is positively related to both nestling growth (Amundsen and Stokland 1990, Magrath 1992, Smith et al. 1995, Amundsen et al. 1996, Hipfner and Gaston 1999, Reed et al. 1999, Styrsky et al. 1999) and nestling survival (Bolton 1991, Blomqvist et al. 1997).

Nestling mass and growth rate are important fitness-related traits because they potentially influence juvenile survival and recruitment (e.g. Tinbergen and Boerlijst 1990, Hochachka and Smith 1991). If egg size affects juvenile survival and recruitment through its effect on nestling mass, there should be an optimum egg size that balances costs of production with benefits to offspring. However, egg size typically varies considerably among females and has a high heritability (Boag and van Noordwijk 1987, Williams 1994, Christians 2002). The apparent paradox of the maintenance of high heritability of egg size in the face of potentially strong selection has been addressed by several authors (e.g. Magrath 1992, Smith et al. 1995, Amundsen et al. 1996, Hipfner and Gaston 1999). One explanation is that selection may act predominantly on the environmental rather than the genetic component of variation in egg size and, thus, not produce an evolutionary response, Price et al. (1988) constructed a quantitative-genetics model that describes a similar phenomenon, the absence of an evolutionary response in breeding date (a heritable trait) despite directional selection for earlier laying in many bird species. Price et al. (1988) demonstrated that a correlation between breeding date and fitness (measured as fecundity) could persist at an evolutionary equilibrium if female nutritional condition (a nonheritable trait) simultaneously affects breeding date and fecundity through separate pathways. Thus, apparent selection for breeding date may actually represent phenotypic selection for female condition and thereby fail to produce an evolutionary response in breeding date. As applied to egg size, Smith et al. (1993) argued that apparent selection for larger eggs in the European Starling (Sturnus vulgaris) might not necessarily reflect genotypic selection because egg size could be affected by environmental conditions mediated by female condition.