7 Pollination Strategies Pollination is the transfer of pollen from an anther to the receptive surface of a stigma within the same species. Most species are hermaphroditic (also known as bisexual) where both male and female parts occur within the same flower. One of the most efficient breeding mechanisms is selfing (autogamy) or self-pollination whereby pollen is accepted by the same flower. Where it does not require a pollinator it is called spontaneous autogamy. The disadvantage is that selfing promotes inbreeding and does not allow for novel combinations of genes as a basis for adaptation to habitat change and speciation. In addition, inbreeding may lead to a decline in plant vigour due to expression of less well-adapted recessive and deleterious genes. Thus, inbreeding may ultimately lead to declining plant vigour within the population. Hence, most species are outbreeders (xenogamy). One way of guaranteeing outbreeding is to have unisexual flowers on separate plants (dioecy). About 5% of southwestern Australian species are dioecious (e.g. Wurmbea dioica (Colchicaceae); Case & Barrett, 2004). Another method is to have male- and female-only flowers on the same plant (monoecy) that accounts for about 3% of SouthWest species (e.g. Diplopeltis, Fig. 7.1) (McComb, 1966). Monoecy only works as an outbreeding device if the opening of the different flower types on a plant is out of phase, as it usually is. Monoecious plants may have hermaphroditic flowers as well as male or female flowers on the same plant. When hermaphroditic and male flowers are present this is known as andromonoecy that occurs within the Proteaceae (e.g. Stirlingia, Ladd & Connell, 1994) and the Myrtaceae (e.g. Melaleuca, Beaufortia) (Beardsell et al., 1993). Nuytsia floribunda (Loranthaceae), the iconic Western Australian christmas tree, is also andromonoecious. Flowers occur in triads, with a central hermaphroditic flower nestled between two functionally male flowers. Thus only one flower sets fruit that sits with its three wings between the three bracteoles that elongate after seed set. When female and hermaphroditic flowers are present it is known as gynomonoecy but it is rare compared with andromonoecy. Trimonoecy occurs when hermaphroditic, male and female flowers are present, and is extremely rare. In a similar manner, dioecious populations can be androdioecious or gynodioecious. © 2015 Philip K. Groom, Byron B. Lamont This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivs 3.0 License. Brought to you by | Graduate School, CAS Authenticated Download Date | 10/10/16 8:15 PM 110 Pollination Strategies Fig. 7.1: (upper) Diplopeltis huegelii (Sapindaceae), a monoecious species (i.e both female and male flowers on the same plant). (left) Female flower, with vestigial stamens that fail to mature, with ovary. (right) Male flower with no style or ovary but prominent stamens. To the left is a fruit with three carpels that developed from the female. Flowers 1 cm wide. (lower) female inflorescences of dioecious Allocasuarina (Casuarinaceae) (left) A. humilis with 5 mm wide inflorescences. (right) A. campestris with 4-cm long cone with woody bracts protecting the fruits to the left of the female inflorescence. Allocasuarina female flowers have long protruding styles that enhance their ability to collect wind-dispersed pollen produced by male flowers on separate plants. 7.1 Outbreeding Strategies Fig. 7.2 outlines various breeding strategies that occur within the SouthWest flora. For outbreeding to be effective, pollen needs to be sourced from another flower (allogamy) − either from the same plant (geitonogamy) or different plants (xenogamy). Geitonogamy only works as an outbreeding device when there are genetic differences within the plant due to somatic mutations that are most likely to occur in plants that live for hundreds of years. To maximise the chance of outcrossing, release of pollen is out of phase with maturation of the stigma (dichogamy) in many hermaphroditic species, and they have evolved a number of strategies to achieve this. Protandry occurs when pollen is shed prior to the stigma becoming receptive and is by far the most common strategy in the Australian flora. Protogyny occurs when the stigma is receptive prior to pollen shedding. Brought to you by | Graduate School, CAS Authenticated Download Date | 10/10/16 8:15 PM Outbreeding Strategies 111 Fig. 7.2: Overview of angiosperm breeding mechanisms. 7.1.1 Protandry Most protandrous families have secondary pollen presentation strategies that involve pollen deposition onto a pollen-presenting organ (Howell, Slater & Knox, 1993) that is exposed to pollinators prior to a receptive stigma developing. To achieve this the anthers and the pollen presenting floral component must be in close proximity to each other prior to anthesis. Howell et al. (1993) recognized nine secondary presentation strategies that included pollen presenters on the apices of styles with concealed (closed or sunken) stigmas (e.g. Proteaceae), sunken stigmas with pollen placed passively (e.g. Polygalaceae), active pollen-placement (e.g. Asteraceae) or indusial (cup-shaped) stigmatic presenters (e.g. Goodeniaceae). Details of how protandry occurs in selected taxa are now considered. 7.1.1.1 Eucalyptus (Myrtaceae) Flowers have numerous stamens arranged in several whorls on the floral cup (hypanthium). In some species the outermost stamens are replaced by staminodes (sterile modified stamens). When the flower opens, the stamens are mature (Fig. 7.3). Once the pollen has been released the spent stamens move outwards; the central stigma then becomes receptive. Brought to you by | Graduate School, CAS Authenticated Download Date | 10/10/16 8:15 PM 112 Pollination Strategies Fig. 7.3: Protandry in the genus Eucalyptus. Photograph is of a recently opened flower of E. caseia, 3 cm wide, with inner stamens erect. 7.1.1.2 Pimelea (Thymelaeaceae) In the open flower the pollen-bearing anthers are held erect above the floral tube (Fig. 7.4), releasing their pollen as a pollinator brushes past the anthers. Over time the spent anthers fall away and the style elongates bearing a receptive stigma. Fig. 7.4: Protandry in the genus Pimelea. Photograph is of Pimelea aeruginosa, capitulum 3 cm wide. 7.1.1.3 Goodeniaceae The family Goodeniaceae is characterized by an indusium, a pollen cup surrounding the stigma (Fig. 7.5). Pollen is shed into this cup that then closes. Anthers wither and the style, bearing the indusium, elongates above the anthers. The stigma now develops, pushing the pollen onto the lips of the indusium. The stigma now spreads, pushing away any remaining pollen, and is pollen receptive. Brought to you by | Graduate School, CAS Authenticated Download Date | 10/10/16 8:15 PM Outbreeding Strategies 113 Fig. 7.5: Protandry in the family Goodeniaceae, showing the function of the indusium. Photographs are of Lechenaultia macrantha (wreath lechenaultia). (left) flower with reddish indusium visible enveloping the hidden stigma, (centre) close up of pollen-laden indusium, (right) entire plant in full flower. Flowers are 2.5 cm diameter, plant 40 cm diameter. 7.1.1.4 Banksia (Proteaceae) The stigma is shielded by a stigmatic groove (or cleft) that is part of the pollen presenter (Fig. 7.6). Pollen is initially deposited onto the presenter at anthesis (as in Grevillea below). Later on, the groove opens revealing the receptive stigma, pushing away any pollen still present around the stigmatic area (Sedgley et al., 1993). There is significant variation among species whether the pollen is deposited over the stigmatic groove in bud or the slit is free of pollen at anthesis (Ladd et al., 1996). 7.1.1.5 Petrophile and Isopogon (Proteaceae) Protandry in both genera occurs by the anthers releasing pollen onto the terminal portion of a distinctively enlarged pollen presenter (Fig. 7.7) atop an elongated style. The terminal portion may be brush-like (e.g. Petrophile linearis; Fig. 7.7) or glabrous (e.g. Isopogon dubius; Fig. 7.7) above which is a stigmatic bulge (Matthews et al., 1999). The swollen basal portion of the presenter may be inversely conical (turbinate) or semi-elliptical. A receptive stigma is formed as the pollen presenter changes colour from yellow to orange-red. This colour change is a signal to pollinators (e.g. native bees) indicating the presence or absence of a reward (pollen) (Lamont, 1985a). Brought to you by | Graduate School, CAS Authenticated Download Date | 10/10/16 8:15 PM 114 Pollination Strategies Fig. 7.6: Protandry in the genus Banksia involves a pollen presenter, a swollen spindle-shaped tip on their elongated styles. Photographs are of B. menziesii (left) with open florets a predominantly yellow colour due to the yellow pollen presenters. Unopen florets are predominantly red due to the colour of the style and perianth. (right) close up of florets at the transition zone (between open and unopened florets) with the yellow pollen presenter (pollen already removed by birds) prominent on the open florets. Fig. 7.7: Pollen presenters in (left) Petrophile linearis and (right) Isopogon dubius. A change in colour, from yellow to orange-red, occurs after the removal of the deposited pollen, and as the stigma becomes receptive. Note pollen grain adhering to tip of pollen presenter in red condition of I. dubius. Pollen presenters 5 mm in length. Brought to you by | Graduate School, CAS Authenticated Download Date | 10/10/16 8:15 PM Outbreeding Strategies 115 7.1.1.6 Grevillea and Hakea (Proteaceae) Flowers have four stamens attached to concavities near the apex of the four segments of the perianth (= floral tube). In the closed flower the tip of the style is nestled among the anthers (Fig. 7.8). The style apex is a swollen and flattened pollen presenter. The presenter surrounds the stigma that is initially submerged and non-receptive. Immediately before the style frees itself from the perianth, pollen is deposited onto the presenter.