The University of Chicago Pollination Efficiency and the Evolution of Specialized Deceptive Pollination Systems. Author(s): Giovanni Scopece, Salvatore Cozzolino, Steven D. Johnson, and Florian P. Schiestl Source: The American Naturalist, Vol. 175, No. 1 (January 2010), pp. 98-105 Published by: The University of Chicago Press for The American Society of Naturalists Stable URL: http://www.jstor.org/stable/10.1086/648555 . Accessed: 04/01/2014 05:37 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp . JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. The University of Chicago Press, The American Society of Naturalists, The University of Chicago are collaborating with JSTOR to digitize, preserve and extend access to The American Naturalist. http://www.jstor.org This content downloaded from 130.92.9.56 on Sat, 4 Jan 2014 05:37:04 AM All use subject to JSTOR Terms and Conditions vol. 175, no. 1 the american naturalist january 2010 ൴ Pollination Efficiency and the Evolution of Specialized Deceptive Pollination Systems Giovanni Scopece,1 Salvatore Cozzolino,1,* Steven D. Johnson,2 and Florian P. Schiestl3 1. Department of Structural and Functional Biology, University of Naples Federico II, complesso Universitario MSA, Via Cinthia, I-80126 Naples, Italy; 2. School of Biological and Conservation Sciences, University of KwaZulu-Natal, P. Bag X01, Scottsville, Pietermaritzburg 3209, South Africa; 3. Institute of Systematic Botany, University of Zu¨rich, Zollikerstrasse 107, CH-8008 Zu¨rich, Switzerland Submitted April 24, 2009; Accepted September 10, 2009; Electronically published November 12, 2009 Online enhancements: appendix tables. der Pijl and Dodson 1966) but also for the unusually com- abstract: The ultimate causes of evolution of highly specialized mon occurrence of species with nonrewarding flowers (i.e., pollination systems are little understood. We investigated the rela- tionship between specialization and pollination efficiency, defined as attracting pollinators by deception; Van der Pijl and Dod- the proportion of pollinated flowers relative to those that experienced son 1966; Dressler 1981; Dafni 1984; Schiestl 2005; Jer- pollen removal, using orchids with different pollination strategies as sa´kova´ et al. 2006): about one-third of all orchid species a model system. Rewarding orchids showed the highest pollination (∼6,500–10,000; according to Ackerman 1986) are non- efficiency. Sexually deceptive orchids had comparably high pollina- rewarding, suggesting an important adaptive advantage of tion efficiency, but food-deceptive orchids had significantly lower this pollination strategy. Most nonrewarding orchids em- efficiency. Values for pollinator sharing (a measure of the degree of ploy generalized food deception to attract their pollinators generalization in pollination systems) showed the reverse pattern, in that groups with high pollination efficiency had low values of pol- (Jersa´kova´ et al. 2006). These species are typically polli- linator sharing. Low pollinator sharing may thus be the basis for nated by a broad assemblage of flower visitors (Dafni 1987; efficient pollination. Population genetic data indicated that both Nilsson 1992; Van der Cingel 1995; Cozzolino et al. 2005). food- and sexually deceptive species have higher degrees of among- A different and less common mode of deception, exclusive population gene flow than do rewarding orchids. Thus, the shift from to the orchid family, is based on attraction of male insects food to sexual deception may be driven by selection for more efficient through mimicry of the visual and olfactory sexual signals pollination, without compromising the high levels of gene flow that are characteristic of deceptive species. of female insects (Kullenberg 1961; Schiestl et al. 1999; Ayasse et al. 2003; Schiestl 2005). An outstanding feature Keywords: food deception, pollination efficiency, pollination strategy, of sexually deceptive orchids is the high level of specificity pollinia, sexual deception, specialized pollination. in their pollination systems, as most species are pollinated by a single species of insect (Paulus and Gack 1990; Bower 1996). Introduction Sexual deception seems to have evolved in different or- Most flowering plants rely on insects for pollination, and chid clades (see Van der Cingel 2001; Jersa´kova´ et al. 2006); the extraordinary evolutionary success of this plant group however, the best-documented evolutionary radiations in- is likely due to the efficiency of animals as pollen vectors, volving transitions to sexual deception are those reported as compared with wind pollination (Pellmyr 2002). While in the Orchidinae and Caladeniinae (Schiestl 2005). Phy- it is often assumed that pollination efficiency (PE) is a key logenetic analyses suggest that food deception is the likely factor for the evolution of pollination systems, compar- ancestral pollination strategy in these groups (Cozzolino ative data on pollen loss in different pollination systems and Widmer 2005) and that some transitions have oc- are scarce. curred between pollination systems. For example, sexual The orchid family is renowned not only for its enormous deception and nectar reward evolved from food deception diversity of pollination mechanisms (Darwin 1862; Van in both the Orchidinae and the Diuridae (Cozzolino et al. 2001; Kores et al. 2001). Similarly, it has been shown for * Corresponding author; e-mail: [email protected]. the South African genus Disa that nectar-rewarding and Am. Nat. 2010. Vol. 175, pp. 98–105. ᭧ 2009 by The University of Chicago. sexually deceptive species evolved from food-deceptive an- 0003-0147/2010/17501-51223$15.00. All rights reserved. cestors (Johnson et al. 1998). The independent occurrence DOI: 10.1086/648555 of these shifts and the apparent concordance in their di- This content downloaded from 130.92.9.56 on Sat, 4 Jan 2014 05:37:04 AM All use subject to JSTOR Terms and Conditions Evolution of Sexual Deception in Orchids 99 rection (from food to sexual deception) suggest a common As yet, comparative data on reproductive performance fitness advantage underlying this change of pollination in these different pollination systems are lacking, thus strategy. However, while a few studies have focused on the making it difficult to infer the driving forces for the evo- fitness implications of deceptive versus rewarding strate- lution of pollination system diversity. The aim of this study gies (Johnson and Nilsson 1999; Smithson 2002; Johnson is to determine the influence of pollination strategy, and et al. 2004; Jersa´kova´ and Johnson 2006), there has been the associated levels of outcrossing, pollinator sharing, and very little progress in uncovering the selective factors that specialization, on the fates of pollen by comparing PE in have driven the shifts from food to sexual deception. multiple populations of food-deceptive, rewarding, and Male mating success in plants depends largely on the sexually deceptive orchid species. fates of pollen. These fates include overall pollen receipt by stigmas, rates of pollen removal, and the overall PE, which can be defined as a ratio of pollinated flowers to Methods the flowers that experienced pollinaria removal (Johnson Data Collection et al. 2004; Tremblay et al. 2005). In orchids, packaging of pollen in discrete pollinia makes it relatively easy to This study was conducted as part of a large survey of estimate pollen removal and deposition (Johnson and Ed- orchid populations of Italy (March–June 2006 and 2007) wards 2000). Pollen fates depend strongly on patterns of and Western Australia (September–October 2007). All the pollinator behavior, which differs among pollination sys- species included in our study belong to the subtribes Or- tems. When visiting rewarding species, for example, pol- chidinae and Caladeniinae and were selected in order to linators tend to restrict their visits to flowers of a single gain a representative sample of each of the three most species (Waser 1986). This so-called flower constancy rep- widespread pollination strategies characterizing this group resents short-term specialization (Grant 1950; Heinrich (i.e., reward pollination, food deception, and sexual de- 1976; Pellmyr 2002) and leads to higher foraging efficiency ception). For the Orchidinae, we analyzed 37 Italian orchid by the pollinator and to a higher probability of intraspecific populations representing 8 genera and 31 species, with 6 pollination for the plant (Free 1963; Waser 1986). How- rewarding species (8 populations), 16 food-deceptive spe- ever, when foraging on rewarding plants, insects also tend cies (19 populations), and 9 sexually deceptive species (10 to visit more flowers per plant and spend considerable populations; table A1 in the online edition of the American time on each flower (Ne’eman et al. 2006). This can lead Naturalist). Field observations were conducted on a total to high levels of pollinator-mediated self-pollination both of 1,911 individuals (8,772 inspected flowers). For the Ca- within and among flowers on a plant (Johnson and Nilsson ladeniinae, in the southwestern part of Western Australia, 1999; Johnson et al. 2004; Jersa´kova´ and Johnson