Evidence that divergent selection shapes a developmental cline in a forest tree species complex

Abstract

Background and aims: Evolutionary change in developmental trajectories (heterochrony) is a major mechanism of adaptation in plants and animals. However, there are few detailed studies of the variation in the timing of developmental events among wild populations. We here aimed to identify the climatic drivers and measure selection shaping a genetic-based developmental cline among populations of an endemic tree species complex on the island of Tasmania.

Methods: Seed lots from 38 native provenances encompassing the clinal transition from the heteroblastic Eucalyptus tenuiramis to the homoblastic Eucalyptus risdonii were grown in a common-garden field trial in southern Tasmania for 20 years. We used 27 climatic variables to model the provenance variation in vegetative juvenility as assessed at age 5 years. A phenotypic selection analysis was used to measure the fitness consequences of variation in vegetative juvenility based on its impact on the survival and reproductive capacity of survivors at age 20 years.

Key results: Significant provenance divergence in vegetative juvenility was shown to be associated with home-site aridity, with the retention of juvenile foliage increasing with increasing aridity. Our results indicated that climate change may lead to different directions of selection across the geographic range of the complex, and in our mesic field site demonstrated that total directional selection within phenotypically variable provenances was in favour of reduced vegetative juvenility.

Conclusions: We provide evidence that heteroblasty is adaptive and argue that, in assessing the impacts of rapid global change, developmental plasticity and heterochrony are underappreciated processes which can contribute to populations of long-lived organisms, such as trees, persisting and ultimately adapting to environmental change.

Fig. 1.

Provenance values for mean effects and associated 95 % confidence intervals for the examined common-garden trial site: (A) vegetative juvenility (i.e. percentage of juvenile foliage retained at age 5 years); and (B) adult survival (i.e. probability of survival at age 20 years). The 38 provenances of the three ontogenetic classes E. tenuiramis (T), E. risdonii (R), and their intermediates (RT) are shown. Provenances have been grouped by ontogenetic class, and then ranked within an ontogenetic class according to the percentage of juvenile foliage previously observed in the wild (Wiltshire et al., 1991, 1998). Ideograms represent the extremes of the phenotypic cline from the heteroblastic E. tenuiramis to the homoblastic E. risdonii ontogenetic classes. The opposite, connate ‘juvenile’ leaf form is retained into reproductive maturity in E. risdonii (bottom), whereas E. tenuiramis is only reproductively mature when bearing the opposite, petiolate ‘adult’ leaf form.

Fig. 2.

Partial dependency plots of the random forest model showing the marginal effect (see Supplementary Data Methods S3 for the description of a marginal effect) of the climate principal components 1 (PC1) and 3 (PC3) on the provenance values for mean effects of vegetative juvenility in the examined common-garden field trial. Three- (A) and two-dimensional (B and C) plots are provided for visualization. For plots B and C, the green arrow shows the location of the trial site along each principal component. Red tick marks show the deciles of the data. The grey shading indicates the 95 % confidence intervals derived by iterative bootstrapping (1000 bootstraps). Increasing scores on PC1 correspond to increasing home-site aridity (high maximum summer temperatures, high radiation and low rainfall), and increasing scores on PC3 correspond to increasing home-site temperatures in general (see Supplementary Data Table S2).

Fig. 3.

Spatial variation in vegetative juvenility across south-eastern Tasmania, as obtained from the random forest model (see also Supplementary Data Table S4) using climate data based on: (A) the contemporary (1976–2005) BIOCLIM surfaces; and (B) BIOCLIM surfaces projected for 2070–2099 using the ECHAM global circulation model (see Supplementary Data Methods S4 and Fig. S3). Also shown is the location of the common-garden field trial (tip of the arrow head) and the River Derwent. The contemporary distribution limit of the E. risdonii–E. tenuiramis complex is depicted by the dotted white line. The inset map shows the geographic position of the expanded region in Tasmania.

Fig. 4.

Based on the applied random forest model (see Supplementary Data Table S4), the figure shows the differences (Δ) in the vegetative juvenility between: (A) the prediction for the common-garden trial site and the estimates for the provenance home sites, both obtained by using the climate data from the contemporary (1976–2005) BIOCLIM surfaces; and (B) the forecasts for the provenance home sites obtained by using the climate data from the BIOCLIM surfaces projected for 2070–2099 (on the basis of the ECHAM global circulation model; see Supplementary Data Methods S4 and Fig. S3) and the estimates for the provenance home sites obtained by using the climate data from the contemporary (1976–2005) BIOCLIM surfaces. Provenance ranking follows the description provided in the legend of Fig. 1.