Heterostyly promotes disassortative pollination and reduces sexual interference in Darwin's primroses: evidence from experimental studies

Abstract

Summary1. Different strategies to reduce selfing and promote outcrossing have evolved in hermaphroditic flowers. Heterostyly, a complex floral polymorphism that occurs in at least 27 families of angiosperms, is hypothesized to achieve both goals by optimizing cross-pollination (via disassortative pollen transfer) and restricting gamete wastage to autogamy (via the reduction in sexual interference between male and female organs). 2. In heterostylous flowers, the reciprocal positioning of sexual organs in different morphs and the pollen incompatibility system within flower or between flowers of the same morph are thought to optimize both male and female functions, reducing the conflicts inherent to the occurrence of both sexual organs in the same reproductive unit. Specific elements of the disassortative-pollination and sexual-interference hypotheses have been tested individually before. However, despite the long-standing interest in heterostyly -ever since Darwin's seminal work on primroses -the predictions derived from these two hypotheses have never been experimentally and systematically examined in the same system. 3. Using distylous primroses (Primula elatior, P. vulgaris), we compare pollen transfer (i) between reciprocal and non-reciprocal flowers; (ii) from anthers onto different parts of the pollinator's body; and (iii) within flower and between flowers of the same morph. We further test whether (iv) anther-stigma distance correlates with self-pollen transfer and whether (v) seed set differs after pollinations with compatible, incompatible and both pollen types. 4. Reciprocal herkogamy promotes differential placement of pollen onto different parts of the pollinator's body, thus effecting transfer of more pollen to reciprocal than to non-reciprocal stigmas and realizing the key predictions of the disassortative-pollination hypothesis. However, short-styled flowers transfer pollen more disassortatively than long-styled flowers in both species, whereas long-styled flowers export more pollen to non-reciprocal than to reciprocal stigmas in P. vulgaris, thus compromising male function in this species. Furthermore, larger distance between sexual organs lowers self-and intra-morph pollination and the pollen incompatibility system decreases seed production after self-pollination, thus diminishing sexual interference. 5. Our results help us understand how the morphological and physiological components of heterostyly contribute to optimizing pollen transfer and minimizing self-and intra-morph pollination, thus promoting more efficient outcrossing in species with this floral polymorphism.

Morpho-anatomical and morphometric studies of the floral structures of the distylous Oldenlandia salzmannii (Rubiaceae)

“…Herkogamy reciprocity is an essential component in models explaining the evolution and maintenance of heterostyly based on enhanced outcrossing (Faivre & McDade 2001). Already in 1877, Darwin proposed that the reciprocal position of the sexual organs in flowers of heterostylous plants would be an adaptation which facilitates pollen exchange between plants of different morphs due to the segregation of pollen in different parts of the pollinator body which is supported by recent studies (Massinga et al 2005;Keller et al 2014). As we mentioned earlier, O. salzmannii presents a high degree of herkogamy reciprocity, but many other distylous species of Rubiaceae present a considerable variation in the distance between style-stigma and stamen heights between morphs, so the herkogamy reciprocity is not perfect.…”

Mixed Mating in Homostylous Species: Genetic and Experimental Evidence from an Alpine Plant with Variable Herkogamy,Primula halleri

“…However, several studies found herkogamy to have a strong genetic basis (e.g., Herlihy and Eckert 2007;Luo and Widmer 2013), and a comprehensive review concluded that the trait is typically highly heritable and evolvable (Opedal et al 2017). Moreover, the profound functional implications of sexual organ position Keller et al 2012Keller et al , 2014Keller et al , 2016) justify speculating about possible adaptive explanations for the existence of high-herkogamous plants.…”

Heterostyly accelerates diversification via reduced extinction in primroses

“…Heterostyly promotes cross-pollination between morphs via delivery and uptake of pollen on distinct parts of the pollinator's body, while preventing or reducing inbreeding via the incompatibility system [40]. The resulting outcrossing mating system [34,38] potentially confers both evolutionary advantages and disadvantages for diversification.…”