Phenotypic plasticity influences the size, shape and dynamics of the geographic distribution of an invasive plant

Abstract

Phenotypic plasticity has long been suspected to allow invasive species to expand their geographic range across large-scale environmental gradients. We tested this possibility in Australia using a continental scale survey of the invasive tree Parkinsonia aculeata (Fabaceae) in twenty-three sites distributed across four climate regions and three habitat types. Using tree-level responses, we detected a trade-off between seed mass and seed number across the moisture gradient. Individual trees plastically and reversibly produced many small seeds at dry sites or years, and few big seeds at wet sites and years. Bigger seeds were positively correlated with higher seed and seedling survival rates. The trade-off, the relation between seed mass, seed and seedling survival, and other fitness components of the plant life-cycle were integrated within a matrix population model. The model confirms that the plastic response resulted in average fitness benefits across the life-cycle. Plasticity resulted in average fitness being positively maintained at the wet and dry range margins where extinction risks would otherwise have been high ("Jack-of-all-Trades" strategy JT), and fitness being maximized at the species range centre where extinction risks were already low ("Master-of-Some" strategy MS). The resulting hybrid "Jack-and-Master" strategy (JM) broadened the geographic range and amplified average fitness in the range centre. Our study provides the first empirical evidence for a JM species. It also confirms mechanistically the importance of phenotypic plasticity in determining the size, the shape and the dynamic of a species distribution. The JM allows rapid and reversible phenotypic responses to new or changing moisture conditions at different scales, providing the species with definite advantages over genetic adaptation when invading diverse and variable environments. Furthermore, natural selection pressure acting on phenotypic plasticity is predicted to result in maintenance of the JT and strengthening of the MS, further enhancing the species invasiveness in its range centre.

Figure 1. Spatial distribution of P. aculeata and survey design according to climate and habitat.

A) Current distribution of P. aculeata across Australia (>800,000 km²) and the survey design across a 1,000 km rainfall gradient. B) Australian locations climatically similar to surveyed sites, as determined using climate-matching function in CLIMEX™ . Within each climate region, populations were surveyed where possible between 2001 and 2007 in three habitat types (defined according to inundation patterns), for a total of 23 populations and more than 3,000 individuals at different life-stages.

Figure 2. Rainfall anomaly histories for the different regions surveyed during the study period (2001–2007).

The rainfall anomaly is the departure from average rainfall conditions (1961–1990). Details on the 23 sites and associated rainfall history can be found in Table S1.

Figure 3. Life-cycle and life-stages of Parkinsonia aculeata.

Nodes represent the three main demographic stages: seed bank (SB), juvenile (Juv: non-reproductive) and adult (Ad). Nodes (continuous lines) represent stages that can be stratified at an annual time step. The adult stage (dashed line) was stratified into 7 sub-stages according to canopy volume: Ad_1.5, Ad₅, Ad₂₀, Ad₅₀, Ad₁₀₀, Ad₂₀₀, Ad₃₀₀ m³: for instance in the volume class A_1.5, trees have a volume between ]1.5 m³–5 m³], and Ad₃₀₀ have volume larger than 300 m². Arcs that link nodes represent the flow of individuals that transit from one stage to another. Self-loops represent the capacity for individuals to delay the transition to the next stage.

Figure 4. Tree-level plastic response between the mass of individual seeds and the number of seeds produced across the rainfall gradient.

A) Reversible plastic tree-level response of the seed mass-seed number trade-off to rainfall. B) Reconstruction of seed mass distribution across the rainfall gradient from 1930 to 2007, using the observed plastic response. C) The most parsimonious tree-level trade-off between seed production and seed mass across the rainfall gradient. Nomenclature - colours correspond to climate regions, as in Figure 1A. Error bars represent s.e.

Figure 5. Benefits of plasticity on fitness components.

A) on seed survival rate (S_seed), and B) on seedling survival rate (S_sg). A, SA, SWT, WT refer to the climate regions (see nomenclature in Fig. 1). For SWT, the Ord site (SWT_Ord) and Auvergne site (SWT_Auv) were analysed separately to account for the difference in S_sg.

Figure 6. Average individual-level fitness benefits of plasticity.

A) The log-normal distribution between annual rainfall and observed fitness (continuous line, average ± s.d) and fitness if there had been no plasticity (dashed line). B) The Jack-of-All-Trades (JT) strategy as predicted from the distribution between annual rainfall and observed probability of extinction (continuous line) and probability of extinction if there had been no plasticity (dashed line). C) Fitness gain provided by plasticity (average ± s.d). D) The Jack-&-Master (JM) strategy as predicted from the correlation between the reduction of probability of extinction and the average fitness benefits. The probability of extinction was calculated as the proportion of the populations with r_s-value<0.

Figure 7. Selection pressure on the plastic trade-off across the annual rainfall gradient, calculated as the sensitivity of average fitness to potential change in the slope (α) and intercept (β) of the trade-off between seed mass and seed number.

Error bars represent s.d. For the riparian habitat in the semi-arid hot and semi-wet tropical region, sensitivities are not stochastic and s.d. represents the variation between years at those sites.