Adaptation to local ultraviolet radiation conditions among neighbouring Daphnia populations

Abstract

Understanding the historical processes that generated current patterns of phenotypic diversity in nature is particularly challenging in subdivided populations. Populations often exhibit heritable genetic differences that correlate with environmental variables, but the non-independence among neighbouring populations complicates statistical inference of adaptation. To understand the relative influence of adaptive and non-adaptive processes in generating phenotypes requires joint evaluation of genetic and phenotypic divergence in an integrated and statistically appropriate analysis. We investigated phenotypic divergence, population-genetic structure and potential fitness trade-offs in populations of Daphnia melanica inhabiting neighbouring subalpine ponds of widely differing transparency to ultraviolet radiation (UVR). Using a combination of experimental, population-genetic and statistical techniques, we separated the effects of shared population ancestry and environmental variables in predicting phenotypic divergence among populations. We found that native water transparency significantly predicted divergence in phenotypes among populations even after accounting for significant population structure. This result demonstrates that environmental factors such as UVR can at least partially account for phenotypic divergence. However, a lack of evidence for a hypothesized trade-off between UVR tolerance and growth rates in the absence of UVR prevents us from ruling out the possibility that non-adaptive processes are partially responsible for phenotypic differentiation in this system.

Figure 1.

Map of the field site, with study ponds labelled in ascending alphabetical order of water transparency. The maximum distance between any two ponds (D–Q) is approximately 1500 m, and the maximum elevation difference is 245 m (800 inch). Ponds overlaid with black/yellow circles are those from which we collected live Daphnia for laboratory experiments, and the degree of shading from black to yellow represents water transparency in 2008. Inset: water clarities of all 17 ponds, estimated from water samples taken in late August of multiple years (filled diamonds, 2006; filled triangles, 2007; filled squares, 2008; filled circles, 2009). Transparencies are the estimated percentage of surface UVR at 10 cm depth. Ponds highlighted in grey match those with overlaid circles on the map. The average coefficient of variation (CV) among all ponds within years is 48%, while the average CV for individual ponds across years is 24%.

Figure 2.

(a) Survival (mean ±s.e.) following ultraviolet radiation (UVR) exposure for D. melanica clones from seven source ponds reared in a common garden. Each point represents a unique Daphnia clone; there are multiple clones per pond. The dashed line represents the UVR transparency model of table 1. (b) Estimated melanin content (mean ±s.e.) of both field-collected and laboratory-raised D. melanica. Olympic laboratory clones are those used in subsequent laboratory experiments. Melanin measures for Sierra Nevada D. melanica [23] are included for reference and have no x-values. Filled circles, Olympic field samples; open circles, Olympic laboratory cultures; filled triangles, Sierra Nevada field samples; open triangles, Sierra Nevada laboratory cultures.

Figure 3.

(a) Inferred ancestry of individual field-collected Daphnia from seven ponds, based on allelic variation at five nuclear microsatellite loci. Vertical bars represent individual animals; the purple proportion represents the ancestry coefficient for cluster 1, orange for cluster 2 and green for cluster 3. Ponds are arranged from left to right in ascending order of ultraviolet radiation transparency; labels correspond to those in figures 1 and 2. (b) Integrated presentation of habitat, phenotype and genetic data. Each vertical bar represents a unique Daphnia clone, with the x- and y-location of the bars as in (a). The shading of each bar represents each clone's ancestry coefficients for the three inferred population clusters, as in figure 2a.

Figure 4.

Estimates of r, the intrinsic rate of population increase, in the absence of ultraviolet radiation (UVR) for a subset of the clones from the UVR tolerance experiments. We use r as a proxy for fitness and find that under standard laboratory conditions there is no relationship between r and a clone's UVR tolerance (linear regression: β = −0.005, p = 0.89, r² = 0.002).