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Speciation, Pattern Recognition and the Maximization of Pollination: General Questions and Answers Given by the Reproductive Biology of the Orchid Genus Ophrys

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Speciation, Pattern Recognition and the Maximization of Pollination: General Questions and Answers Given by the Reproductive Biology of the Orchid Genus Ophrys Journal of Comparative Physiology A (2019) 205:285–300 https://doi.org/10.1007/s00359-019-01350-4 REVIEW Speciation, pattern recognition and the maximization of pollination: general questions and answers given by the reproductive biology of the orchid genus Ophrys Hannes F. Paulus1 Received: 21 March 2019 / Revised: 17 May 2019 / Accepted: 18 May 2019 / Published online: 28 May 2019 © The Author(s) 2019 Abstract Pollination syndromes evolved under the reciprocal selection of pollinators and plants (coevolution). Here, the two main methods are reviewed which are applied to prove such selection. (i) The indirect method is a cross-lineage approach using phylogenetical trees to understand the phylogeny. Thus, features of single origin can be distinguished from those with multiple origins. Nearly all pollination modes originate in multiple evolutionary ways. (ii) The most frequent pollinators cause the strongest selection because they are responsible for the plant’s most successful reproduction. The European sexually decep- tive orchid genus Ophrys provides an example of a more direct way to prove selection because the attraction of a pollinator is species specifc. Most members of the genus have remarkably variable fowers. The variability of the signals given of by the fowers enables the deceived pollinator males to learn individual fower patterns. They thus avoid already visited Ophrys fowers, interpreting them as females rejecting them. As the males will not return to these individually recognizable fowers, the pollinators´ learning behavior causes cross-pollination and prevents the orchid’s self-pollination. Keywords Selection · Reproductive success · Ophrys · Learning behavior Introduction consideration have a look in Chittka and Thomson (2001) or Waser and Ollerton (2006). Most advances in pollination biology have resulted from These approaches refect the two historic starting points interdisciplinary research combining ecological and evolu- for the discipline. One approach emphasized detailed obser- tionary perspectives. Several approaches have been essen- vation of foral mechanisms and the natural history of the tial for understanding the functional ecology of foral traits, ecological relationships between plants and pollinators. It the dynamics of pollen transport, competition for pollinator originated with pioneering work by Sprengel (1793) and services, and patterns of specialization and generalization in Müller (1873). An interesting second approach focuses on plant–pollinator interactions. Understanding plant–pollinator evolutionary processes that might afect and be afected by interactions requires and invites a variety of viewpoints and pollination. Pollinators act as selection factors attracted by conceptual approaches, ranging from descriptions of animal signals emitted by the fower to increase its reproductive behavior and their contributions to pollination success to fo- success above that of other individuals of the same species. ral evolution. Many of the results of evolutionary approaches Some plants operate with signals similar to sexual traits in in pollination biology are summarized in some very informa- a pollinator´s courtship behavior to attract it and to thereby tive textbooks (Harder and Barrett 2006; Willmer 2011) or guarantee fertilization. The specifc patterns of pollinator the many special articles in Patiny (2011); for a more special visitation infuence important aspects of the pollinator´s mating system and minimize self-pollination of the plant. A special case in this respect is the sexual deception by some orchid genera like that by the European Ophrys spe- * Hannes F. Paulus cies (Pouyanne 1917; Kullenberg 1961, 1973; Paulus 2006, [email protected] 2007; Schiestl 2011). 1 Department of Integrative Zoology, Faculty of Life Sciences, University of Vienna, Althanstr.14, 1090 Vienna, Austria Vol.:(0123456789)1 3 286 Journal of Comparative Physiology A (2019) 205:285–300 General questions Evolution of fower signals Research in pollination biology has been at the forefront of The rapid expansion of insect pollination was due to the theory testing and model building. In evolutionary biology, emergence of “clever” attractants, such as fower shape pollination systems have provided some of the best tests of connected with colored displays and many diferent scents. theories of evolution by natural selection and the adaptive The fower colors were selected by the pollinators, co- nature of foral traits (Levin 1985; Campbell 1985; Camp- evolving with their visual system (Schiestl and Johnson bell et al. 1996; Schemske and Bradshaw 1999). One of the 2013). There must have been strong competition between main questions in this respect is whether pollinators act as the early fowers for insects and later also other pollina- selective partners triggering most of the fower evolution. tors. As a consequence, the signals evolved in many dif- There are two diferent ways to fnd answers: (i) one mainly ferent directions. The motivation of the fower visitors had comes from reconstructions of phylogeny and evolution- to be rewarded with food. In most cases, this is protein- ary processes (e.g. DeWitt Smith 2010), (ii) the other relies rich pollen and nectar, providing simple sugars such as on measurements of reproductive success as a function of fructose, saccharose and glucose. These are ideal energy pollinator behavior (e.g. Paulus 1988, Gervasi and Schiestl suppliers which can be directly transferred into muscle 2017). The origin of pollination modes in specifc plants activity during fight. Bees (Apoidea) evolved shortly after can possibly be explained using the results of phylogenetical the fowering plants and diversifed into higher lineages trees. These can help to understand how often and in which contemporaneously with the radiations evolving within ways a particular pollination syndrome evolved. A quantita- the angiosperms. Major bee lineages (i.e., families) were tive measure of selective pressures mainly needs long-term presumably established by the late Cretaceous (Cardinal observations in the feld or even better experimental work. and Danforth 2013; Cappellari et al. 2013; Plant and Pau- lus 2016; Sann et al. 2018). Bees visit fowers not only to Flowers and their specifc pollination modes feed themselves. Instead, they are specialised in collecting and storing pollen and nectar, as food for their larvae. This Most of the angiosperm fowers require help in transport- signifcantly increased the frequency of fower visits. Bees ing their pollen to the stigma of another fower of the same evolved to be very efcient pollinators and most of the species. They borrow it from diferent animals (zoogamy: angiosperm species today are pollinated by one or several pollination by animals; entomogamy: pollination by insects). of the many hundreds of diferent bee species. As a con- Exceptions are species pollinated by wind (anemogamy) sequence of the competition for pollinators, the rich diver- (most gymnosperms, secondarily some groups of angio- sity of today’s fower types has evolved which also trig- sperms) or obligate selfers (autogamy). In Europe, most gered multiple evolutions of new pollinator animals. This pollinators are insects. Many of them are very selective process of reciprocal selection is accompanied by many regarding the fowers visited. reciprocal adaptations (Gilbert and Raven 1975; Paulus Whereas most angiosperms have hermaphroditic fow- 1978; Janzen 1980). The result is a remarkable diversity ers, gymnosperms primarily have separate male and female in butterfies, bees, fower visiting birds or bats, which fowers. They use the wind for pollination. To ensure fertili- would have never evolved without their fowers. Because zation, male fowers have to produce enormous amounts of of the development of more and more specialised pollina- pollen grains. As pollen contains a lot of nitrogen, a strongly tion methods, signals had to become more diferentiated. limited resource, its production is a costly process. Pollina- As bees, like most insects, are able to see colors, even UV, tion by insects evolved during the early Mesozoic era, possi- fowers developed many diferent color patterns and indeed bly frst by some of the pollen-eating beetles which had been UV patterns which we as human beings are unable to see well established since the Perm period. As some beetles fed (Dyer et al. 2012). Many of these UV patterns together on the seeds of gymnosperms, some of these developed with yellow markings are interpreted as imitation of the sheets protecting their seeds, which became a crucial char- stamina or the two-lobed anther because they mainly occur acteristic of the later angiosperms. Pollen feeding alone was on fowers with hidden androecium. Therefore, these spots not enough to ensure pollination as these beetles visited only are replacement signals instead of the normally visible the male fowers. Female fowers were not attractive, as nec- stamens (Osche 1979, 1983; Paulus 1988; Lunau 1990, tar evolved much later. The solution was to evolve bisexual 2000; Lunau et al. 2017). Importantly, when interpreting fowers, the next special characteristic of most angiosperms. the color of a particular fower we always have to ask for the visual system of the pollinator. The same applies to all the other sensory modalities. Olfactory fower signals in most cases help the pollinator to fnd fowers at larger 1 3 Journal of Comparative Physiology A (2019) 205:285–300 287 distances. Another feld of research comes from fndings
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