Floral adaptation and diversification under pollen limitation

Abstract

Pollen limitation (PL) of seed production creates unique conditions for reproductive adaptation by angiosperms, in part because, unlike under ovule or resource limitation, floral interactions with pollen vectors can contribute to variation in female success. Although the ecological and conservation consequences of PL have received considerable attention in recent times, its evolutionary implications are poorly appreciated. To identify general influences of PL on reproductive adaptation compared with those under other seed-production limits and their implications for evolution in altered environments, we derive a model that incorporates pollination and post-pollination aspects of PL. Because PL always favours increased ovule fertilization, even when population dynamics are not seed limited, it should pervasively influence selection on reproductive traits. Significantly, under PL the intensity of inbreeding does not determine whether outcrossing or autonomous selfing can evolve, although it can affect which response is most likely. Because the causes of PL are multifaceted in both natural and anthropogenically altered environments, the possible outcrossing solutions are diverse and context dependent, which may contribute to the extensive variety of angiosperm reproductive characteristics. Finally, the increased adaptive options available under PL may be responsible for positive global associations between it and angiosperm diversity.

Figure 1.

Graphical model of (a) the limits on total seed production and (b) the reproductive transitions considered in the model of selection on reproductive traits (which also considers outcross siring success). Panel a illustrates combinations of cross-fertilization (F_x) and self-fertilization (F_s) that result in PL (white area below diagonal), ovule limitation (heavy diagonal line) and resource limitation (grey area) of seed production (areas above the diagonal are not possible) given that 30 and 80% of selfed and outcrossed zygotes survive genetic death to become embryos (i.e. g_s = 0.3, g_x = 0.8), maternal plants have sufficient resources to mature 60% of their ovules into seeds (R/O = 0.6) and the probability that selfed seeds establish reproductive offspring is 70% that for outcrossed seeds (d_s/d_x = 0.7). The arrows projecting from the black, grey and white symbols illustrate examples of possible directions of evolution under pollen, ovule and resource limitation, respectively, and the associated equations relate necessary conditions for inbreeding depression. The slope of the dashed line projecting from the origin is F_x/F_s, which is a selection threshold under resource limitation (see equation (4.3)). The black dashed line through the pollen-limited (i.e. black) point is its associated fitness isocline: selection can move the mating system only to the right of this isocline. The grey dashed line through the same point is the seed-production isocline. In panel (b) the height of each block depicts the number of entities (pollen, zygotes, etc.) during each reproductive stage, with white and grey areas representing outcrossed and selfed fractions, respectively.

Figure 2.

Graphical models of the effects of (a) variation in pollen import (i) on mean seed production (s; based on Richards et al. 2009) and (b) variation in pollinator abundance (n) on the expected optimal allocation to pollinator attraction (a; inspired by Burd 2008). The black curve in each panel depicts the relation of the dependent to the independent variable. The solid grey line maps the mean independent variable into the corresponding value of the dependent variable and the dashed grey lines map low (L) and high (H) values of the independent variable that are equally spaced below and above the mean independent variable. Because seed production increases nonlinearly with pollen import, mean seed production for variable pollen import () is less than the fecundity expected given the mean pollen import (s′), both of which are lower than the maximum possible seed production, indicating PL. Richards et al. (2009) referred to the difference between s′ and as variance limitation. Similarly, because the optimal allocation to pollinator attraction declines nonlinearly with pollinator abundance, the average optimal allocation to attraction () is less than the optimum expected for average pollinator abundance (a_HW), which is equivalent to the balance between pollen and resource limitation predicted by Haig & Westoby (1988), resulting in chronic PL.

Figure 3.

Relation between the mean (±s.e.) effects of habitat fragmentation on pollination and female fecundity for 23 self-compatible (dashed line) and 27 self-incompatible (solid line) species (modified from Aguilar et al. 2006). Effect size was measured by Hedge's d. Reanalysis by ANCOVA detected a positive relation of fecundity to pollination success (F_{1, 46} = 7.95, p < 0.01), but this effect did not differ significantly between self-compatible and self-incompatible species (compatibility class, F_{1, 46} = 1.60, p > 0.2; interaction, F_{1, 46} = 0.76, p > 0.3). Open circle, self compatible; filled circle, self-incompatible. The grey diagonal line indicates equal effect sizes for pollination and fecundity.