Pollination intensity and paternity in flowering plants

Abstract

Background: Siring success plays a key role in plant evolution and reproductive ecology, and variation among individuals creates an opportunity for selection to act. Differences in male reproductive success can be caused by processes that occur during two stages, the pollination and post-pollination phases of reproduction. In the pollination phase, heritable variation in floral traits and floral display affect pollinator visitation patterns, which in turn affect variation among plants in the amount of pollen exported and deposited on recipient stigmas. In the post-pollination phase, differences among individuals in pollen grain germination success and pollen tube growth may cause realized paternity to differ from patterns of pollen receipt. The maternal plant can also preferentially provision some developing seeds or fruits to further alter variation in siring success.

Scope: In this review, we describe studies that advance our understanding of the dynamics of the pollination and post-pollination phases, focusing on how variation in male fitness changes in response to pollen limitation. We then explore the interplay between pollination and post-pollination success, and how these processes respond to ecological factors such as pollination intensity. We also identify pressing questions at the intersection of pollination and paternity and describe novel experimental approaches to elucidate the relative importance of pollination and post-pollination factors in determining male reproductive success.

Conclusions: The relative contribution of pollination and post-pollination processes to variation in male reproductive success may not be constant, but rather may vary with pollination intensity. Studies that quantify the effects of pollination and post-pollination phases in concert will be especially valuable as they will enable researchers to more fully understand the ecological conditions influencing male reproductive success.

Keywords: Floral traits; male reproductive success; paternity; pollen competition; pollen limitation; pollen sorting; pollination; pollination intensity; pollinator; post-pollination; sexual selection; siring success.

Fig. 1.

Genetic and ecological factors influencing pollination and post-pollination processes in hermaphroditic flowering plants. The relative importance of each of these processes in determining plant fitness depends on a variety of factors and the interplay between them. These factors may include: pollinator abundance, amount of pollen transferred, resource availability and maternal seed provisioning. These factors are discussed in detail throughout this review.

Fig. 2.

Pollen germinating on a Mimulus ringens stigma. Note that a few grains are not hydrated, and only some of the grains have formed pollen tubes. Pollen grains are 15–25 µm in diameter. Image: Wendy Semski.

Fig. 3.

Pollen sorting as a function of the intensity of pollination. The three pistils in the diagram represent low, medium or high pollen loads. The coloured dots on each stigma represent equal numbers of pollen grains from four different pollen donors. These donors differ in speed of pollen tube growth, with red fastest, followed by yellow, light blue and purple (slowest). Unfertilized ovules are small and white; fertilized ovules are larger and coded by the colour of the pollen donor. Illustration: Allysa Hallett.

Fig. 4.

Predicted relationships between pollination intensity and (A) variance in pollination success, (B) variance in male reproductive success (RS) during the post-pollination phase, and (C) overall variance in male siring success including both pollination and post-pollination influences.