The evolution of alternative mechanisms that promote outcrossing in Annonaceae, a self-compatible family of early-divergent angiosperms

Abstract

Annonaceae flowers are generally hermaphroditic and show high levels of outcrossing, but unlike many other early‐divergent angiosperms lack a self‐incompatibility mechanism. We reassess the diversity of mechanisms that have evolved to avoid self‐pollination in the family. Protogyny occurs in all hermaphroditic flowers in the family, preventing autogamy but not geitonogamy. Herkogamy is rare in Annonaceae and is likely to be less effective as beetles move randomly around the flowers in search of food and/or mates. Geitonogamy is largely avoided in Annonaceae by combining protogyny with floral synchrony, manifested as either pistillate/staminate‐phase synchrony (in which pistillate‐phase and staminate‐phase flowers do not co‐occur on an individual) or heterodichogamy (in which two phenologically distinct and reproductively isolated morphs coexist in populations). Unisexual flowers have evolved independently in several lineages, mostly as andromonoecy (possibly androdioecy). Functionally monoecious populations have evolved from andromonoecious ancestors through the loss of staminate function in structurally hermaphroditic flowers. This has been achieved in different ways, including incomplete pollen/stamen development and delayed anther dehiscence. Angiosperms display an enormous diversity of mechanisms to promote xenogamy, many of which are easily overlooked without fieldwork. Floral phenology is particularly important, especially cryptic differences in timing of organ maturation or abscission. © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174, 93–109.

Floral Biology and Pollination Ecology ofDesmos chinensis(Annonaceae): Assessing the Efficacy of Floral Synchrony for Promoting Xenogamy

“…Inter-and intraindividual floral synchrony were investigated by surveying 10 individual plants over 10 consecutive days in the Ho Sheung Heung population in the summer of 2008 (Pang and Saunders 2014). The simultaneous occurrence of pistillate-, interim-, and staminate-phase flowers within and between individual plants was determined.…”

“…Self-incompatibility has been implicated as one of the key evolutionary innovations that enabled the rapid diversification of angiosperms during the Cretaceous (Whitehouse 1950;Zavada and Taylor 1986;Igic et al 2008) and is likely to have evolved independently in different lineages (Charlesworth et al 2005) since different genetic control mechanisms exist, expressed in either the gametophytic or the sporophytic generations (Allen and Hiscock 2008). Self-incompatibility has been shown to be lacking in many early-divergent angiosperms, however, including the Amborellaceae and some Nymphaeales and Magnoliales, such as the Annonaceae and Magnoliaceae (Bernhardt and Thien 1987;Dieringer and Espinosa 1994;Allen and Hiscock 2008;Pang and Saunders 2014). It has been hypothesized that the deleterious genetic consequences arising from the absence of self-incompatibility in these early-divergent lineages may be offset by selective advantages arising from the ability to reproduce under unfavorable conditions, such as isolated populations where there are constraints on the number of genetically distinct individuals and periods where pollinator availability is limited (Barrett and Eckert 1990;Lloyd 1992;Goodwillie et al 2005;Pang and Saunders 2014).…”

“…Self-incompatibility has been shown to be lacking in many early-divergent angiosperms, however, including the Amborellaceae and some Nymphaeales and Magnoliales, such as the Annonaceae and Magnoliaceae (Bernhardt and Thien 1987;Dieringer and Espinosa 1994;Allen and Hiscock 2008;Pang and Saunders 2014). It has been hypothesized that the deleterious genetic consequences arising from the absence of self-incompatibility in these early-divergent lineages may be offset by selective advantages arising from the ability to reproduce under unfavorable conditions, such as isolated populations where there are constraints on the number of genetically distinct individuals and periods where pollinator availability is limited (Barrett and Eckert 1990;Lloyd 1992;Goodwillie et al 2005;Pang and Saunders 2014). Selfcompatible early-divergent angiosperms have nevertheless been shown to exhibit a diversity of alternative mechanisms that promote outcrossing (xenogamy) by reducing self-fertilization and biparental inbreeding, including intrafloral dichogamy (the temporal separation of pistillate and staminate function in hermaphroditic flowers), herkogamy (the spatial separation of pollen presentation and receipt in hermaphroditic flowers), floral 1 Author for correspondence; e-mail: saunders@hku.hk.…”

“…All rights reserved. 1058-5893/2015/17604-0003$15.00 DOI: 10.1086 synchrony, and the evolution of structurally or functionally unisexual flowers (Endress 2010;Pang and Saunders 2014). Achieving high levels of xenogamy is clearly of considerable importance, even in plants that are self-compatible.…”

“…Malmeoideae tribe Maasieae (Maasia; Rogstad 1994, as Polyalthia) and subfam. Annonoideae tribes Annoneae (Annona; Murray and Johnson 1987, as Rollinia;Lora et al 2011), Guatterieae (Guatteria;Webber 2002), and Uvarieae (the Dasymaschalon-Desmos-Friesodielsia clade; Pang and Saunders 2014;X. Guo, personal communication).…”