Quantitative genetics, together with multivariate selection theory, provides a poweril framework with which to understand adaptive phenotypic evolution in nature. To date, information on the genetic basis of phenotypic traits in nature has come from those few populations where inheritance could be estimated using traditional quantitative genetic techniques. Newer, molecular marker-assisted methods promise to allow the estimation of quantitative inheritance in previously inaccessible, natural populations that display interesting patterns of phenotypic evolution. Here, I utilized a natural avian population, the Capricorn silvereye (Zosterops lateralis chlorocephalus) to: firstly, investigate the genetic basis of traits underlying evolution towards increased body size following colonization of an island from the continental mainland; and secondly, test the utility of marker-based approaches to estimating quantitative inheritance in wild populations.
A cross-fostering experiment was used to estimate the additive genetic variance-covariance (G) matrix for six morphological traits describing body and culmen size and shape, in two consecutive cohorts of silvereye nestlings. Significant levels of additive genetic variance were found for three traits. The lowest levels of genetic variance were detected for tarsus length and culmen depth, two traits which show the largest phenotypic shift in the evolution from the mainland to the island phenotype. Genetic correlations among traits were high and positive and suggestive of modularization of beak and body size, which may facilitate shape changes in island silvereye subspecies. The G matrices for the two cohorts were highly similar, which suggested short-term stability of the genetic variance-covariance matrix.
The extent and form of natural selection were estimated and the phenotypic response to selection was predicted for each cohort. Significant linear and non-linear selection was detected, in both years, on culmen traits, particularly culmen depth. Linear selection gradients differed significantly between cohorts, with different traits being favoured in different years. The predicted responses to selection were positive and in the direction of mainland-island phenotypic differentiation, that is, towards increased body size. The genetic covariance structure underlying these morphological traits may be constraining evolution to this particular direction.
Molecular marker approaches to estimating inheritance in natural populations rely on inferring relatedness between individuals. A species-specific microsatellite library was constructed and over one hundred other avian primers investigated in order to infer relatedness in the silvereye, resulting in a set of eleven polymorphic microsatellite loci. This set of markers was found to reliably estimate genetic relationships, in conjunction with the Queller & Goodnight (1989) relatedness estimator, by testing inferred relatedness against genetic relationships determined from field observations.
Ritland's (1996) method was used to estimate a molecular marker-assisted G matrix by analysing the co-variation of inferred relatedness and phenotypic trait similarity between individuals. The molecular marker-assisted G was compared to the G matrix estimated from the cross-fostering experiment using a multivariate, matrix framework. The marker-assisted method resulted in imprecise and inaccurate estimates of genetic variances and covariances, with some traits having negative variances and marker-assisted estimates being substantially smaller than values obtained from the cross-fostering analysis. Common environment inflated phenotypic resemblance, but the full extent to which it could confound estimates of variances and covariances could not be ascertained using a cross-fostered data set. However, the two G matrices were highly similar, indicating that the marker-assisted method retained overall matrix covariance structure and that it may provide a way of estimating G matrix structure in nature.
This study illustrates the power of quantitative genetic approaches in elucidating the roles of the underlying genetic variance-covariance structure and natural selection in microevolutionary processes in a silvereye population. Marker-based approaches may expand the scope of quantitative genetic analyses to other natural populations, particularly in the estimation of G matrix structure. Further research is needed into the utility of marker-based approaches if quantitative genetics is to provide a powerful framework for understanding adaptive phenotypic evolution in nature.