Aging in a long-lived clonal tree

Abstract

From bacteria to multicellular animals, most organisms exhibit declines in survivorship or reproductive performance with increasing age ("senescence"). Evidence for senescence in clonal plants, however, is scant. During asexual growth, we expect that somatic mutations, which negatively impact sexual fitness, should accumulate and contribute to senescence, especially among long-lived clonal plants. We tested whether older clones of Populus tremuloides (trembling aspen) from natural stands in British Columbia exhibited significantly reduced reproductive performance. Coupling molecular-based estimates of clone age with male fertility data, we observed a significant decline in the average number of viable pollen grains per catkin per ramet with increasing clone age in trembling aspen. We found that mutations reduced relative male fertility in clonal aspen populations by about 5.8 x 10(-5) to 1.6 x 10(-3) per year, leading to an 8% reduction in the number of viable pollen grains, on average, among the clones studied. The probability that an aspen lineage ultimately goes extinct rises as its male sexual fitness declines, suggesting that even long-lived clonal organisms are vulnerable to senescence.

Figure 1. Male fertility declined significantly with increasing clone age.

Relative clone sexual fitness was measured as the average number of pollen grains per catkin per ramet, divided by the estimated ancestral mean fitness (from the absolute value of the intercept of 17,456). In this figure we present both the results of a multiple regression and those from a simple linear regression with a single predictor, clone age, based on glacial calibration. (a) From a simple linear regression, we found the estimated slope was −8.1×10⁻⁵ (F _1,18 = 10.41, p = 0.005, R ² = 0.33, 95% CI: −1.3×10⁻⁴ to −2.8×10⁻⁵). Dashed curves represent the 95% confidence intervals around the fitted line. A randomization test confirmed the significance of this relationship (Figure S5, p = 0.025). (b) Results from a multiple linear regression confirm that male sexual fitness declines with clone age.

Figure 2. Male fertility and asexual fitness measures are not significantly related.

(a) At the ramet level, there was no evidence for a trade-off between growth rate as measured by volume growth per year (m ³ per year) and ramet male fertility (r = 0.04, t = 0.388, df = 94, p = 0.70). (b) Although a correlation analysis between maximum distance between two ramets in a clone, D_max, and the clone's mean male fertility was significant (r = −0.55, t = −2.762, df = 18, p = 0.013), this relationship was sensitive to the inclusion of a single data point (indicated by a circle). (c) Removing this point, the relationship is no longer significant (r = −0.40, t = −1.802, df = 17, p = 0.09).