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

• Published in: Functional ecology Vol. 28; no. 6; pp. 1413 - 1425
• Main Authors: Keller, Barbara, Thomson, James D, Conti, Elena, Kudo, Gaku
• Format: Journal Article
• Language: English
• Published: Oxford British Ecological Society 01.12.2014; John Wiley & Sons Ltd; Wiley-Blackwell; Wiley Subscription Services, Inc
• Subjects: Animal and plant ecology; Animal, plant and microbial ecology; anthers; Autoecology; autogamy; Biological and medical sciences; breeding system; distyly; floral polymorphism; flowers; Fundamental and applied biological sciences. Psychology; gamete wastage; General aspects; hermaphroditism; male and female functions; morphs; outcrossing; Plant-animal interactions; Plants and fungi; plant–insect interaction; pollen; pollination; prediction; Primula; Primula elatior; Primula vulgaris; reciprocal herkogamy; seed set; selfing; breeding system; Insecta; distyly; Male; male and female functions; Primula; plant―insect interaction; Plant; Female; Flower; Interference; Experimental study; Pollination; Mating system; Gamete; selfing; Animal plant relation; gamete wastage; Arthropoda; Heterostyly; reciprocal herkogamy; outcrossing; Invertebrata; Polymorphism; floral polymorphism
• ISSN: 0269-8463; 1365-2435
• DOI: 10.1111/1365-2435.12274

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). 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. 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. 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. 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.