A tale of two morphs: modeling pollen transfer, magic traits, and reproductive isolation in parapatry

Abstract

The evolution of the flower is commonly thought to have spurred angiosperm diversification. Similarly, particular floral traits might have promoted diversification within specific angiosperm clades. We hypothesize that traits promoting the precise positional transfer of pollen between flowers might promote diversification. In particular, precise pollen transfer might produce partial reproductive isolation that facilitates adaptive divergence between parapatric populations differing in their reproductive-organ positions. We investigate this hypothesis with an individual-based model of pollen transfer dynamics associated with heterostyly, a floral syndrome that depends on precise pollen transfer. Our model shows that precise pollen transfer can cause sexual selection leading to divergence in reproductive-organ positions between populations served by different pollinators, pleiotropically causing an increase in reproductive isolation through a "magic trait" mechanism. Furthermore, this increased reproductive isolation facilitates adaptive divergence between the populations in an unlinked, ecologically selected trait. In a different pollination scenario, however, precise pollen transfer causes a decrease in adaptive divergence by promoting asymmetric gene flow. Our results highlight the idea that magic traits are not "magic" in isolation; in particular, the effect size of magic traits in speciation depends on the external environment, and also on other traits that modify the strength of the magic trait's influence on non-random mating. Overall, we show that the evolutionary consequences of pollen transfer dynamics can depend strongly on the available pollinator fauna and on the morphological fit between flowers and pollinators. Furthermore, our results illustrate the potential importance of even weak reproductive isolating barriers in facilitating adaptive divergence.

Figure 1. Conceptual “cartoons” of the effects of reproductive-organ height on the transfer of pollen between distylous flowers.

Arrows show directions of pollen flow, arrow widths show magnitude of expected fertilization, and dashed red circles indicate the region with the highest probability of pollen deposition. A: Pollen transfer between well-matched reciprocal morphs. Pollen donated at the low position by a pin is transferred to a low position on the pollinator's body and arrives at a low position in the recipient thrum; similarly, pollen donated at a high position by a thrum arrives at a high position in the recipient pin. Because pollen arrives at the height of the recipient stigma and is compatible with it, fertilization is likely to occur. B: Hindrance of pollen transfer between reciprocal morphs poorly matched in their reproductive-organ heights. Due to this mismatch, pollen arrives at the wrong height and is thus less likely to be received by the stigma and result in fertilization. The height mismatch thus causes some degree of reproductive isolation.

Figure 2. Pollinator stickiness functions used in the presented results.

The x-axis represents the corolla tube height (0 = bottom, 1 = top) at which the pollen grain encounters the pollinator's body. The y-axis represents the probability that the pollen grain will stick to the pollinator at that height. A: The “uniform” pollinator, with equal, maximal stickiness at all heights. B: The “high-biased” pollinator, which is not sticky at all below a threshold height, and then is increasingly sticky with increasing height. C: The “bimodal-low” pollinator, which is sticky principally at two distinct positions on its body. D: The “bimodal-high” pollinator, which is sticky principally at two distinct positions different from those of the “bimodal-low” pollinator.

Figure 3. Reproductive-organ–height mismatch, reproductive isolation at fertilization, and ecological divergence as a function of the pollinator crossover probability, strength of selection, and precision of pollen transfer for scenario 1, involving the pollinator pair “bimodal-low” + “bimodal-high”.

For all panels, colors and plot symbols represent the strength of selection. For panels D–F, line dashing indicates the patch depicted (1 or 2), but the two patches respond essentially identically in this scenario. Columns correspond to levels of pollen transfer precision: left is precise, σ _j = 0.01; center is intermediate, σ _j = 0.1; right is imprecise, σ _j = 0.5. The x-axis in all panels represents the pollinator crossover probability, c, from allopatry (c = 0.0) to sympatry (c = 0.5). Gray lines and symbols in all panels show the control runs corresponding to the (colored) treatment runs. Error bars show ±SE, which is often too small to be visible. Top row (A–C): The y-axis shows the magnitude of spatial mismatch between reciprocally placed sexual organs of the two floral morphs. Center row (D–F): The y-axis shows the degree of reproductive isolation present at fertilization, an indication of the strength of sexual selection against non-local pollen (i.e., mechanical isolation); note this metric also includes the temporally prior effect of geographic isolation. Bottom row (G–I): The y-axis shows the extent of ecological divergence between populations.

Figure 4. Reproductive-organ–height mismatch, reproductive isolation at fertilization, and ecological divergence as a function of the pollinator crossover probability, strength of selection, and precision of pollen transfer for scenario 2, involving the pollinator pair “uniform” + “high-biased”.

Colors, symbols, error bars, dashing, columns, rows, and axes are as in Fig. 3.

Figure 5. Asymmetrical dynamics of adaptation and reproductive function for scenario 2, involving the pollinator pair “uniform” + “high-biased”.

Colors, symbols, error bars, dashing, and columns are as in Fig. 3. The x-axis in all panels represents the pollinator crossover probability, c, from allopatry (c = 0.0) to sympatry (c = 0.5). Top row (A–C): The y-axis shows the degree of adaptation to the local optimum in patch 1, , which ranges from complete local adaptation (+1.0) to complete maladaptation (−1.0; e.g., complete adaptation to the optimum of the other patch). Middle row (D–F): The y-axis shows the degree of adaptation to the local optimum in patch 2, , ranging from +1.0 to−1.0 as for the top row. Bottom row (G–I): The y-axis shows the mean female function, calculated as the percentage of available ovules filled at the end of the pollination phase.

Figure 6. Increase in local adaptation as a function of the pollinator crossover probability, strength of selection, and precision of pollen transfer for both scenarios.

Top row (A–C): scenario 1, involving the pollinator pair “bimodal-low” + “bimodal-high”. Bottom row (D–F): scenario 2, involving the pollinator pair “uniform” + “high-biased”. The increase in local adaptation is defined as the difference between the mean local adaptation in treatment realizations and the mean local adaptation in corresponding control realizations with the same parameter values (where the local adaptation in patch i is defined as , as in Fig. 5). Positive and negative values thus represent increased and decreased adaptation, respectively, in treatment realizations relative to controls. Colors, symbols, error bars, dashing, columns, rows, and axes are as in Fig. 3.