Botany Letters

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Letters to the twenty-first century botanist: “What is a flower?” (3) The flower as an evolutionary arms race: was Linnaeus’s choice misleading?

Marc-André Selosse

To cite this article: Marc-André Selosse (2016) Letters to the twenty-first century botanist: “What is a flower?” (3) The flower as an evolutionary arms race: was Linnaeus’s choice misleading?, Botany Letters, 163:3, 231-235, DOI: 10.1080/23818107.2016.1198988

To link to this article: http://dx.doi.org/10.1080/23818107.2016.1198988

Published online: 30 Jun 2016.

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Download by: [179.216.183.86] Date: 05 October 2016, At: 09:30 Botany Letters, 2016 VOL. 163, NO. 3, 231–235 http://dx.doi.org/10.1080/23818107.2016.1198988

LETTER Letters to the twenty-first century botanist: “What is a flower?” (3) The flower as an evolutionary arms race: was Linnaeus’s choice misleading?

Marc-André Selossea,b aMuséum national d'Histoire naturelle, Département Systématique et Evolution (UMR 7205 ISYEB), Paris, France; bDepartment of Plant Taxonomy and Nature Conservation, University of Gdansk, Poland

ARTICLE HISTORY received 4 June 2016; Accepted 5 June 2016

In this series of ‘Letters to the twenty-first century bota- emerges from a pile of dead, counter-selected and less nist’ dedicated to the flower (Dodinet and Selosse 2016), optimal interactions that may have existed in the past. Nadot and Dodinet (2016) established a first definition Animal-pollinated flowers combine three kinds of based on morphology and supported by evo-devo. features. The first feature, relevant for plant reproduc- Dodinet (2016) then challenged this view by propos- tion, is production of pollen, which must be deposited ing the ethnobotanist’s perspective, and evidencing the on or harvested from the animal vectors. The second variability of perception of the flower depending on the feature is relevant on the animal side: it is the reward, ethnographical context. But even in the framework of most often a nutritional one, but sometimes a shelter. western science, not every scientific community sees The third and last feature allows animal attraction, and the flower in the same way. The current essay seeks to concerns flower shape, size, colour, odour and timing bring an evolutionist’s outlook to the multiple ways of of anthesis (Faegri and Van der Pijl 1979), or even its approaching and defining the flower. I first describe the surface microstructure (Whitney et al. 2009). Yet these flower in co-evolution with animals, entailing an accel- features are not necessarily linked to each other: the

eration of evolution by an arms race; then I show that reward (most of the time, sugar) is not conspicuous or the diversity of flowers provided tools for classification, attractive in itself as it has no colour or odour so that especially for Linnaeus’s scheme, fully based on flowers; flowers are attractive by aposematism, i.e. only after ani- finally, I describe how a phenomenon arising from fast mals are selected by floral features, or gain experience co-evolution, namely convergence, makes flower shapes with the signals displayed; pollination is independent often irrelevant as criteria for families retrieved by mod- of the reward for the animal, which allows cheating ern, phylogenetic classifications. (animals can pollinate without reward, or take the reward without pollinating). Indeed, this allows evolu- Flower as a battlefield tionary conflicts, where one partner does not pay the reward linked to the interaction, such as nectar-free, but About 80% of plants are pollinated by animals (Abrol attractive flowers (for instance, 30% of orchid species 2012), so the flower is involved in an interaction with are rewardless; Jersakova, Johnson and Jürgens, 2009; animals such as insects, birds or mammals in the vast Selosse 2014) or non-pollinating animals that rob nec- majority of flowering plants. A naive view is that of a per- tar (Inouye 1983). Although the impact of cheaters on fect matching and complementarity between animals, fitness (= number of offspring) of the partners is variable seeking food or resting or even breeding sites, and flow- (e.g. Maloof and Inouye 2000), such cheaters pave the ers, which ensure out-crossing thanks to animal vectors way for the emergence of truly parasitic species (Sachs (Figure 1A). Indeed, beyond morphological diversity, and Simms 2006). Moreover, floral cheating repeatedly the functional analysis of flowers reveals various ways evolves (e.g. Chartier, Gibernau and Renner 2014). that allow, and often optimize, the interaction with ani- Hence, many flower features can be viewed as second- mals (Proctor, Yeo and Lack 1996). Yet this is a story arily selected to enforce animal cooperation, as a result of winners because many protagonists of plant–animal of co-evolution with pollinators and cheater avoidance. floral interactions probably went extinct in the past, and For example, in Salvia spp. flowers, the fused corolla the feeling of an optimization as observed nowadays and calix as well as the stamen with a lever mechanism

CONTACT Marc-André Selosse [email protected] © 2016 Société botanique de France 232 M.-A. Selosse

Figure 1. Flowers as manipulators of pollinators. (A) Salvia ssp. flowers illustrate a mechanism adapted to pollinator behaviour, where access to the nectar, prevented on the lateral sides by fused corolla and calix, forces the animal (here modelled by a pen) to act on a lever mechanism that bends the two stamens, connected together at their midpoint, onto the back of insects, or onto the beak of birds. (B–E) Buzz-pollinated, salt-shaker-like flowers from unrelated families, respectively (B) Sowerbaea laxiflora (Asparagaceae), (C) Platytheca galioides (Elaeocarpaceae), (D) Thomasia macrocarpa (Malvaceae) and (E) Borago officinalis (Boraginaceae). Red arrows: poricidal opening.

(Figure 1A) all force animals to receive pollen on their classification in the Systema naturae (Linnaeus 1753, way to nectar, situated at the base of the corolla tube. 1758; Figure 2) on flowers that vary a lot and provide Rather than a marvellous complementarity with animal many criteria due to their complexity. Although most partners, the zoogamous flower is a battlefield where authors before him used floral criteria for classification, only the survivors, more or less adapted to the partners, his system is exclusively based on flowers (Figure 2); and more or less avoiding cheaters, can be observed. moreover, it is also based on a seductive interpretation of Tomorrow, a new trait in one species may promote the the flower, derived from precursors such as Camerarius emergence of new cheaters, or better cheating avoid- and Tournefort (Vallade 2008), which survives today and ance. Flowers have to adapt to both abiotic and biotic made his classification popular: the flower is the place changes, the latter being a selective force that, according for mating, hence the name ‘sexual system’ for Linnaeus’s to the Red Queen hypothesis (Van Valen 1973), acceler- classification. Nowadays, in a different exercise, plant ates evolutionary rates because the partners’ evolution identification, we still use flowers (with few exceptions, proceeds faster than abiotic environmental changes. see Eggenberg and Mohl 2013), a fact probably In other words, flowers may evolve faster, especially in explained by both the intrinsic variability of flowers terms of morphology, than other organs because of an and an inheritance of Linnaeus’s emphasis on flowers. evolutionary arms race with pollinators. Flowers track Yet, purely in terms of classification, a close look at the evolution of their partners in a continuous co-­ Figure 2 reveals how our current view of classification has evolution, but can also shift to new partners (Whittle changed. Linnaeus distinguished flowers where sexuality and Hodges 2007). is invisible (Clandestinae) versus visible (Publicae). In the latter, Diclina have unisexual flowers while Monoclina have hermaphroditic flowers with male and female Flower diversity and Linnaeus’s classification parts on the thalamus that are either close (Affinitas) Floral shapes are more diverse than, for example, the or separate (Diffinitas). Within the latter, one section is shapes of leaves, which are less directly involved in biotic subdivided on the basis of the number of stamens (Mon-, interactions, and this may result in a faster evolutionary Di-, Triandria, etc.; Figure 2). exploration of possible shapes and functioning. This is This emphasizes the outstanding contribution of precisely where Linnaeus was efficient: he based his flowers to the eighteenth century classification, but Botany Letters 233

Figure 2. Linnaeus’s classification of plants: the ‘Key to the sexual system’ from the 10th edition of Systema Naturae (Linnaeus, 1758). also how things have changed since then, as Linnaeus’s into account, but also the evolutionary status of traits, classification of plants did not survive. Indeed, at that derived (apomorphic) or ancestral (plesiomorphic), is a time, classification was rather a description of what God post hoc product of the analysis (see discussion in Selosse created, in a fixist view of Nature, as shown in Linnaeus’s and Durrieu 2004). Many categories homogeneous in words Deus creavit, Linnaeus disposuit (“God created, the Systema naturae turned out to be polyphyletic, Linnaeus organized”). Nowadays, classifications take because they relied on traits that emerged repeatedly. into account a fundamental characteristic of living For example, unisexual flowers evolved independently beings: evolution. Having evolved and sharing more or thousands of times (Renner 2016). Ironically, this system, less ancient common ancestors with other species, living which was the big disponendum target of Linnaeus, is beings can be classified according to this specific property, now forgotten, whereas we have retained the binomial which creates various levels of relatedness (Selosse and naming of species, names that were trivial in his eyes, Durrieu 2004). The so-called phylogenetic system is best entirely factitious and good only until specific essential exemplified by the work of the ‘Angiosperm Phylogeny names could be established (Selosse 2011). Group’ (APG III 2009; APG IV 2016). Not only are more To be fair, let us say that Linnaeus himself considered diverse characters (predominantly molecular) now taken that his system was artificial, and that ‘artificial systems 234 M.-A. Selosse are entirely necessary as long as we lack a natural one’ Flowers are no longer flagships for high-level (Linnaeus 1735). Yet the importance of flowers in clas- taxa sifications survived Linnaeus and the eighteenth century, Hence, similar-looking flowers do not necessarily together with the fact that their role in plant sexuality belong to phylogenetically related plants. First, unre- often meant that their role in biotic interaction was seen lated clades may exhibit convergence; second, due to as secondary, or even overlooked. fast evolution, related species may differ in floral shape. In the examples above of sympetaly or buzz-pollinated Evolutionary saturation and convergences in salt-shaker-like flowers, few or no families are homo- floral evolution geneous for the focus floral appearance. At least in In the arms race with pollinating animals, acceleration of the zoogamous groups, the flower is labile and chang- evolution can be expected to result in the repeated emer- ing because it is an active co-evolutionary battlefield. gence of similar organizations and underlying strategies, Whereas the flower is a good species marker, it is not a phenomenon called evolutionary saturation. Several necessarily a good marker for higher taxonomic levels, traits may have undergone saturation. For example, the e.g. the family. Although some flower types may clearly fusion of the corolla, or sympetaly, once used to define identify a given family, not all members of the family the Sympetalae, characterizes the so-called “Asterids”, share this type of flower. but it is sporadically present in Monocots (e.g. some In this sense, Linnaeus’s choice to classify plants Burmanniaceae), basal eudicots (some Menispermaceae exclusively on the basis of flowers and their sexuality, and Delphinium in Ranunculaceae), and Rosids (e.g. although relevant in his time of fixism, did not pre- Crassulaceae, Malvaceae) (Endress 2011). As stated pare subsequent generations for a phylogenetic, evo- above, this may be interpreted as a way to drive ani- lutionary classification. Because floral characters often mals to nectar by way of the sexual parts of the flower show poor phylogenetic conservatism due to the arms (Figure 1A). race, high-level taxa are no longer easily identifiable by Many other pollinating mechanisms arose repeat- flower shape. This aspect of modern phylogenetic clas- edly: the buzz-pollinated salt-shaker-like flowers pres- sifications still often bothers students and their teach- ent a suite of traits that evolved jointly and repeatedly ers. However, this is not fully new: the Ranunculaceae (Figure. 1B–E). Flowers are bent on one side with more and Rosaceae families have long since been acknowl- or less fused petals, which prevents any access to the edged without a unifying flower shape. One lesson is underside where nectar is produced; anthers are joined that most conspicuous features such as flowers, taken together with poricidal dehiscence (opening by a termi- alone, are often misleading when defining high-level nal hole; Figure 1C,D), and the mature pistil emerges in taxa. Another lesson is the need to pay more attention the centre of the anther group. This fertile column is the to vegetative criteria, which are sometimes neglected place where insects hang on, but, since it offers limited by botanists, but which may offer a better phylogenetic gripping ability, the animals keep flying and generate conservatism. vibrations that release the pollen or allow its deposi- … and last but not least, coming back to a defini- tion on the pistil (Proctor, Yeo and Lack 1996). Such tion of flowers for the twenty-first century botanist: the flowers are known from some (but not all) Annonaceae, flower is often a battlefield, and a place for an active, fast Asparagaceae (Figure. 1B), Boraginaceae (Figure 1E), co-evolution with pollinators. Elaeocarpaceae (Figure 1C), Ericaceae (sensu lato), Malvaceae (Figure 1D), Primulaceae, Gesneriaceae, Acknowledgements Solanaceae, etc. They show that several traits, at first Marc-André Selosse is supported by the Fondation Ars glance independent (flower shape and bending, pori- Cuttoli & Paul Appell, and the Polish National Science cidal dehiscence), may evolve jointly within a common Centre (Maestro7-NZ project Orchidomics). He sincerely function, making convergence often morphologically acknowledges P. Selosse, E. Dodinet and S. Nadot for complex. discussions, D. Marsh for English corrections, and dedicates this paper to the memory of the late Guy Durrieu, Another highly convergent trait is the existence of ut in tristitia persiteat amicitiam memoriamque. multiple (often yellow) stamens, which is interpreted as a way of attracting pollen-eating pollinators such as beetles (Proctor, Yeo and Lack 1996): this strategy ensures that Disclosure statement insects interact with the pollen, and aligns the reward No potential conflict of interest was reported by the author. and the pollination, but at the expense of a large loss of pollen. More generally, pollination experts recognize Notes on contributor the so-called “pollination syndromes” (Ashworth et al. 2015), i.e. convergent evolution towards similar forms Marc-André Selosse is a professor at Muséum national d’ among various plants that target the same guild of pol- Histoire naturelle and in universities of Gdansk (Poland) linators, in a loose form of convergence. and Viçosa (Brazil). 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