Testing limits to adaptation along altitudinal gradients in rainforest Drosophila

Abstract

Given that evolution can generate rapid and dramatic shifts in the ecological tolerance of a species, what prevents populations adapting to expand into new habitat at the edge of their distributions? Recent population genetic models have focused on the relative costs and benefits of migration between populations. On the one hand, migration may limit adaptive divergence by preventing local populations from matching their local selective optima. On the other hand, migration may also contribute to the genetic variance necessary to allow populations to track these changing optima. Empirical evidence for these contrasting effects of gene flow in natural situations are lacking, largely because it remains difficult to acquire. Here, we develop a way to explore theoretical models by estimating genetic divergence in traits that confer stress resistance along similar ecological gradients in rainforest Drosophila. This approach allows testing for the coupling of clinal divergence with local density, and the effects of genetic variance and the rate of change of the optimum on the response to selection. In support of a swamping effect of migration on phenotypic divergence, our data show no evidence for a cline in stress-related traits where the altitudinal gradient is steep, but significant clinal divergence where it is shallow. However, where clinal divergence is detected, sites showing trait means closer to the presumed local optimum have more genetic variation than sites with trait means distant from their local optimum. This pattern suggests that gene flow also aids a sustained response to selection.

Figure 1

The relationship between altitude and the site mean of CCT for (a) the Kirrama (72 isofemale lines) and (b) Paluma transects (74 isofemale lines). Error bars represent standard errors. The linear regression at Kirrama is significant (F_1,8=8.52, p=0.019; R²=0.52). Sites represented by less than five lines are represented by open squares.

Figure 2

The mean number of D. birchii males caught per day (filled squares) and the mean daily temperature (open circles) at each site of a given altitude along (a) the Kirrama and (b) Paluma transects. Error bars on density estimates represent the standard error.

Figure 3

Sites whose trait mean are different from the presumed optimum are associated with lower between-isofemale line variance compared with those close to the optimum along the Kirrama ecotone. Deviations from optima are the absolute distances between the site mean and the fitted line for the significant regression for CCT observed at Kirrama (figure 1). The correlation is significant (r=−0.67, p=0.048). Sites represented by less than five isofemale lines are represented by open squares.