The evolution of postpollination reproductive isolation in Costus

Abstract

Reproductive isolation is critical to the diversification of species. Postpollination barriers may be important in limiting gene flow between closely related species, but they are relatively cryptic and their evolution is poorly understood. Here, we review the role of postpollination reproductive isolation in plants, including the various stages at which it operates and the hypotheses for how it may evolve. We then review empirical studies in the plant genus Costus, evaluating documented postpollination barriers in light of these hypotheses. We summarize isolation due to parental style length differences and present evidence supporting the hypothesis that the differences are in part a by-product of selection on floral morphology. Additionally, we show that reduced pollen adhesion, germination, and tube growth contribute to reproductive isolation between two closely related sympatric species of Costus. Geographic variation in the strength of these crossing barriers supports the hypothesis that they evolved under reinforcement, or direct natural selection to strengthen isolation.

Keywords: Costus; Postpollination; Reinforcement; Reproductive isolation.

Fig. 1

Relative seed set residuals plotted against style length differences for 26 interspecific pairings of Costus species. This graph shows the relationship between style length difference and crossing success while controlling for genetic distance and putative cases of reinforcement of pollen–stigma incompatibility. Style length significantly affects relative seed set in this combined model (P < 0.001). Relative seed set values (heterospecific seed set/conspecific seed set) were truncated at 1.0 and arcsine square root transformed before statistical tests. See Kay and Schemske (2008) for crossing details

Fig. 2

The majority rule consensus tree constructed from the posterior distribution of trees. Pollination syndrome and corolla length were reconstructed using parsimony. In lineages with hummingbird pollination, corolla length decreases (with the exception of C. stenophyllus). Photographs by Kay and Schemske

Fig. 3

Postpollination isolation between sympatric C. pulverulentus and C. scaber, adapted from Kay (2006). a The number of germinated pollen grains for C. scaber as the maternal parent with C. scaber and C. pulverulentus as pollen donors. Differences in pollen adhesion and percent germination combine to give an overall difference in the number of germinated pollen grains per pollination. b For C. pulverulentus as the maternal parent, differences in the final length of the pollen tubes contribute to a large difference in the number of pollen tubes reaching the ovary. The dashed line represents the average style length of C. pulverulentus, and therefore the total distance pollen tubes need to grow. Costus scaber pollen tubes do not grow the length necessary to reach the C. pulverulentus ovary

Fig. 4

Map depicting the locations of C. pulverulentus and C. scaber and the relative success of the interspecific crosses, adapted from Kay and Schemske (2008). Arrows point in the direction of pollen transfer. Heavy arrows indicate higher crossing success (>60% relative seed set), and light arrows indicate poor crossing success (<30% relative seed set)

Fig. 5

Pollen tube growth rates (mm/h) for intraspecific and interspecific crosses of C. pulverulentus and C. scaber plants from La Selva