Floral colour change as a potential signal to pollinators

Floral colour change as a potential signal to pollinators

Available online at www.sciencedirect.com ScienceDirect Floral colour change as a potential signal to pollinators Graeme D Ruxton1 and H Martin Schae...

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Available online at www.sciencedirect.com

ScienceDirect Floral colour change as a potential signal to pollinators Graeme D Ruxton1 and H Martin Schaefer2 Colour change in flowers (with age and/or after pollination) is taxonomically widespread, has evolved repeatedly, and has a range of putative selective benefits linked to modifying pollinator behaviour; however, this phenomenon seems paradoxically uncommon. We explore this paradox by reviewing the empirical evidence and argue that the evolution and maintenance of floral colour change as a signal to modify pollinator behaviour require special ecological circumstances that will often not be met across a plant population for a sustained number of generations, which potentially explains the scarcity of this phenomenon. We discuss alternative explanations for floral colour change and potentially fruitful lines of future research. Addresses 1 School of Biology, University of St Andrews, St Andrews KY16 9TH, UK 2 Faculty of Biology, University of Freiburg, Department of Evolutionary Biology and Animal Ecology, Hauptstr. 1, 79104 Freiburg, Germany Corresponding author: Ruxton, Graeme D ([email protected])

Current Opinion in Plant Biology 2016, 32:96–100 This review comes from a themed issue on Biotic interactions Edited by Consuelo De Moraes and Mark Mescher

http://dx.doi.org/10.1016/j.pbi.2016.06.021 1369-5266/# 2016 Published by Elsevier Ltd.

Introduction Flower colouration is an important mediator of interactions between plants and their animal pollinators. Some flowers change colour with age and/or after successful pollination, and this colour change influences subsequent behaviour of pollinators [1]. These changes in pollinator behaviour have often been argued to provide selective benefits to the plant; it therefore seems paradoxical that floral colour change is taxonomically widespread occurring in at least 38% of the angiosperm orders but only in the minority of the species in each of them [2]. Recently, Ohashi et al. proposed that flower colour changes occur more frequently, particularly in the UV range of the spectrum that early studies did not account for [3] but still considered it as an unusual phenomenon. Here, we explore the evolutionary ecology of floral colour change with particular emphasis on explaining why it has apparently evolved many times but remains uncommon [2,4]. Current Opinion in Plant Biology 2016, 32:96–100

Potential benefits of floral colour change In this section, we argue that the current evidence and logical reasoning point to a narrow range of circumstances under which floral colour change is sufficiently beneficial to evolve and be maintained through often-suggested benefits in terms of modification of pollinator behaviour. We consider these benefits in turn. First, it has been suggested that floral colour change can increase the rate of pollinator visitation at the whole-plant level. We agree that there is evidence that the retention of old flowers can increase long-range attraction of pollinators towards the whole plant. However, there is no strong evidence or logical reason why this is enhanced by colour change in older flowers (see [1,5–9]). Turning to another suggested benefit, if old flowers are retained, floral colour change can direct pollinators preferentially towards the rewarding flowers and thereby reduce pollinators’ probability of leaving the plant early. There is empirical evidence that this behaviour can increase the fitness of plants. For example, bees biased their visits to rewarding flowers in the colour-changing Weigela coraeensis but not in the co-occurring non-colour-changing species W. hortensis with a similar pattern of nectar availability [10]. Importantly, seed set in W. coraeensis reached 95% and could not be increased by artificial pollination, whereas seed set in W. hortensis was much lower (27%) and could be increased by artificial pollination. Thus, we agree that this study suggests that floral colour change can enhance fitness by directing pollinators to the rewarding flowers (see also [6,8]). However, in general, we expect that the selective benefits to the plant through this mechanism will vary depending on the extent to which pollinators are limited and the neighbourhood effect of how alternative floral rewards affect pollinator behaviour. We thus consider that likely spatio-temporal variation in floral resources and pollinator abundance will mitigate against strong and consistent selection pressure for floral colour change through this mechanism. This same spatiotemporal variation will also hinder its long-term maintenance if colour change is costly. Potential costs include the production of enzymes for the synthesis for pigments, modulation of pH values, transport of molecules into cell vacuoles, and aromatic acylation [10,11]. Further, if floral colour change is costly, it is only expected to evolve as a signal to pollinators if cues (such as volatiles or humidity) that are necessary by-products of rewards [12] are not already reliable indicators of floral rewards. Finally, colour change could also be selected because it promotes outcrossing and decreases geitonogamous www.sciencedirect.com

Understanding floral colour change Ruxton and Schaefer 97

pollination. For example, experimentally removing pollen from receptive flowers reduced the reliability of the colour-reward relationship of these flowers and reduced pollinator visitation and seed set [13]. Specifically, when the pollinator first arrives at a plant, it potentially carries pollen from a different conspecific plant; this will likely be deposited on the first few flowers visited on the focal plant. Thus, a signal might be particularly valuable when it influences the pollinator, so that the first few visits of the pollinator within the focal plant enable reproductively active flowers to exploit this pollen. Additionally, if the last few visited flowers on the plant are reproductively active, then pollen can be gathered from them. The pollen load a pollinator carries when leaving the plant is thus higher than that after having visited non-viable flowers where pollen may be lost without fitness benefit to the plant. Again, both these gene-transfer benefits to floral colour change have empirical support (e.g. [8,14,15,16]) and can be seen as a refinement of the above-mentioned mechanism of directing pollinators to unpollinated flowers. Thus, they are similarly logically valid but are also likely to be similarly influenced by spatio-temporal variation in pollinator density and neighbourhood effects. Additionally, the extent of temporal separation of male and female functions to prevent selffertilisation; the relative effectiveness and availability of own and foreign pollen; and variation between pollinator types (and environmental conditions) in pollen collection, retention and deposition will affect selection pressure for floral colour change through this mechanism. In summary, we suspect that the evolution and maintenance of floral colour change through modifying pollinator behaviour require special ecological circumstances that will often not be met across a plant population for a sustained number of generations, which potentially explains the scarcity of this phenomenon (Figure 1).

Other factors that could influence costs and benefits of floral colour change One hypothesis on floral colour change is that independent of spatio-temporal variation in the pollinator community, colour change exploits the innate colour preferences of pollinators that are consistent across plant taxa. This hypothesis is supported by consistent preferences for white over purple flowers by both native syrphids and introduced bumblebees in a New Zealand alpine (Euphrasia dyeri Wettst.) that shows white-to-purple floral colour change [17]. However, colour preferences are often transient and malleable according to the local colour-reward relationships and thus dependent upon spatio-temporal variation in floral resources. Transient colour preferences are explicable by the extraordinary speed of honeybees in colour learning, which is not just superior to human infants but to all vertebrates studied so far [18]. Thus, even though pollinators have innate colour preferences, it is not clear whether these are consistent enough in space and time to drive the evolution of flower www.sciencedirect.com

Figure 1

Current Opinion in Plant Biology

A large bee-fly (Bombylius major) visits the flowers of the lungwort Pulmonaria officinalis. This species changes the colour of its flowers from red to blue-violet. The colour change is produced by a change in the pH of cell vacuoles from acidic to alkaline, which changes the anthocyanin pigments from the red, flavinium cation form to neutral quinonoidal bases. # Claudia Gack.

colour change. Likewise, seed dispersers within days develop colour preference rankings depending on the local fruit supply [19], suggesting that innate biases of plant mutualists are quickly overridden by their experience of local food supply. Although we have focussed on floral colour change as a potential signal associated with changing rewards as a flower becomes rewardless, volatile signals are also possible. Schiestl and Ayasse describe volatile emissions by a sexually deceptive orchid Ophrys shegodes [20]. After pollination, the flowers produce farnesyl hexanoate. In dualchoice tests, flowers artificially scented with that compound were significantly less attractive than controls. This compound is found on the cuticle of only mated females of the pollinating bee Andrena nigroaenea. However, the quantities produced by the flowers are orders of magnitude less than that produced by female bees; this is perhaps because the plant needs to avoid neighbouring (unpollinated) flowers to also become unattractive if a given flower produces high levels of this aversive compound. To us, it seems likely that visual signals rather than volatile signals are selected to indicate unrewarding flowers because visual signals are spatially more precise than olfactory signals. Structural changes to flowers may also be important in directing pollinators; Fusato et al. [21] recently showed that flowers of the perennial Gentiana triflora var japonica closed after a pollinator visit. They further showed that the fraction of closed flowers had no effect on the plant’s Current Opinion in Plant Biology 2016, 32:96–100

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long-range attractiveness to pollinators, but that closed flowers were less preferred in close-range choice tests. In considering selection for floral colour change, we should remember that colour change may have consequences and are indeed evolutionary drivers unrelated to pollinators: Pelabon et al. [22] recently showed that floral colour change from white to green was associated with enhanced photosynthesis and carbon delivery to developing seeds.

Possible facultative use of floral colour change As discussed above, we think it is very likely that the relative costs and benefits of floral colour change will often be highly variable among plant populations. Some sources of this variation (such as sunlight, temperature and soil condition as mediators of the cost of pigment production) may be readily detectable by plants. Thus, it is feasible that plants use colour change facultatively (i.e. only under suitable conditions). This has been unexplored, but there is evidence of phenotypic plasticity in colour change: Jabbari et al. [23] found that in the protandous weed Saponaria officinalis, floral colour change was coincident with a switch from male to female functioning. However, they also found that colour change (through the production of anthocyanins) was much more pronounced in plants exposed to direct sunlight than in those grown in the shade, which is explicable as anthocyanin synthesis is often controlled by the availability of light [24]. It is not clear whether this plasticity is adaptive, and indeed, it is yet to be shown that pollinators are responsive to floral colour change in this species. However, the facultative use of floral colour change remains worthy of further investigation.

Possible importance of floral colour change in the evolution of relationships with different pollinators Another underexplored area is the evolutionary potential of floral colour change. Floral colour change can be a precursor for changes in the pollinator spectrum. The colour change from yellow to red after pollination has occurred can be an important evolutionary transition towards the evolution of red flowers that are often associated with bird pollination [25]. Maraconesian Lotus spp. have evolved the ability for colour change following anthesis at least three times from yellow flowers to red, purple or brown flowers [25]. Interestingly, these authors suggest that red floral colour in this genus (which is likely associated with pollination by birds) has evolved from facultative red flowers that changed their colour once pollination has occurred. This is a plausible suggestion and similar cases may occur more widely. That is, the developmental colour change originally selected for its influence on insect pollinators may be a pre-adaptation to an evolutionary transmission to a bird pollination syndrome involving the Current Opinion in Plant Biology 2016, 32:96–100

loss of papillate cells [26]. Even more generally, the machinery involved in floral colour change may be a pre-adaptation to evolution of floral appearance in response to many distinct selection pressures such as changing light regimes associated with changes in the canopy or competition for pollinators among flowering species. Thus, although we have suggested that sensitivity to ecological conditions may lead to frequent evolutionary loss of floral colour change, its ease of initial evolution may still allow it to play an important evolutionary role through facilitating diversity in floral pigmentation. As outlined above, an alternative hypothesis for rarity of floral colour changes might be that the evolution of floral colour change is ephemeral over evolutionary time, because it represents an intermediate step in the unidirectional evolutionary transition from insect to bird pollination of a particular species. In this scenario, species with floral colour changes (mostly yellow-orange flowers or white-blue flowers) represent the transition from the ancestral insect pollination (white and yellow flowers) to more derived bird pollination (purple to red flowers). This hypothesis could be tested using a phylogenetic comparative approach. Rausher [27] suggested that in at least two major angiosperm taxa, Penstemon and Ipomoea, evolutionary transitions from blue to red flowers, usually associated with transitions from bee to bird pollination, are highly correlated with changes in the class of pigment produced. Current understanding of the anthocyanin biosynthetic pathway in turn indicates that this change in pigment type is most likely due to inactivation of one or more of the major branches of that pathway.

Useful avenues for future research in floral colour change There are some potentially effective approaches to understand the evolution of floral colour change that we feel are unjustly neglected in the current literature; we have therefore highlighted them at the end. It would be very valuable to have a greater understanding of the genetic basis of colour changes (e.g. genes linked to the production of pigments or the metabolic pathways linked to the changes in colour) or information on the cell activity (behaviour of the metabolites associated with colour changes) associated with this phenomenon. Further, comparative phylogenetic approaches could be used to disentangle the various alternative hypotheses by exploring whether floral colour change’s independent evolution is linked to factors such as changes in nectar production, flower size and shape, pollinator type, or habitat (for example). A recent example of this is the comparative study of 219 species by Ohashi et al. [3], who concluded that pigment chemistry and reduced colour contrast at a short range — when modelled in insect vision — reduce potential benefits of floral colour change in terms of modifying pollinator behaviour and thus help to explain the low prevalence of colour change. The issue of floral www.sciencedirect.com

Understanding floral colour change Ruxton and Schaefer 99

colour contrast against the background was also explored recently by Brito et al. [28] who suggested that a combination of differently coloured and aged flowers enhanced the overall attraction of pollinators to a distance in a massively flowering tree Tibouchina pulchra. Consistent with the effects of contrasts, experimental evidence suggests that display size and flowering patterns can further influence the effects of floral colour changes [29]. Although conducted in a non-natural setting, the recent work by Suzuki and Ohashi [9] discussed earlier provides a novel, comprehensive hypothesis to explain why species with colour-changing and non-colour-changing flowers both prevail: colour changers will be successful only when the benefits through modifying the behaviour of pollinators outweigh the costs of colour change. In contrast, when plants under environmental stress can increase pollinator visits solely by enhancing conspicuousness, the hypothesis of these authors predicts that cost saving can become advantageous. They compared details of trait combinations and pollination consequences for a colourchanging species (W. coraeensis) and a non-colour-changing sister species (W. hortensis) in a shared environment. They found that the colour changers attracted more pollinators. The two species do not co-occur in the natural world, and the colour changers occur in environments where the authors expect competition for pollinators to be more intense and photosynthesis rates (and thus the ability to invest in anthocyanins for colour changing or for protecting tissue in the senescent flower analogous to the appearance of anthocyanins in senescent leaves) to be higher. Their results strongly support the idea that we need to compare trait combinations and their multiple functions between closely related species to understand the evolution of floral colour change. For this particular comparison, the demonstration of a cost to colour change would be a valuable step forward. It is of course well known that vision is not the only sensory system used by pollinators in influencing their interaction with flowers, and multimodality seems an important aspect of floral signalling [30–32]. It would be useful to explore whether there are concomitant changes in volatile emission from flowers that are associated with floral colour change; whether such changes influence pollinator behaviour; and in particular, whether responses by pollinators appear to combine information gathered through different sensory systems such that the floral changes can be interpreted within the recently developed general theory underlying multimodal signalling [33,34]. Similarly, the genetics of floral colour are increasingly well understood [35,36]. Interestingly, one to two mutations within the colour pathways can produce categorical colour shifts, such as those among blue and red anthocyanins and red and yellow carotenoids. For example, the shift from ancestral blue to red flowers in the genus Ipomoea and Petunia is produced by one or two loss-of-function mutations and www.sciencedirect.com

lead to a shift in pollinators [37,38]. These studies show why floral colouration can be an evolutionary labile trait as it may be determined by few genes with large effects on pollinator attraction. It would be particularly useful to better understand the genetic basis for floral colour change involving distinct pigments and model systems. This would allow better characterisation of potential costs of such colour change, and potentially allow the development of genetically modified (GM) variants where we can control the nature and timing of floral colour change and explore its consequences for seed set or other appropriate metrics of plant fitness.

Conclusions We suspect that the evolution and maintenance of floral colour change through modifying pollinator behaviour require special ecological circumstances that will often not be met across a plant population for a sustained number of generations, which potentially explains the scarcity of this phenomenon. However, a fuller understanding of the evolutionary pressures on floral colour change requires not just consideration of the benefits to plants in terms of modifying pollinator behaviour, but also the costs, other physical changes, cues and signals that could influence pollinator behaviour and evolutionary pressures unrelated to pollinator behaviour. Excitingly, the recent research that we highlight is helping transition the field to this more holistic approach, and we hope that this review will focus and accelerate that transition.

Author contributions Both authors conceived the structure of this article and contributed to writing it. No other persons are entitled to authorship.

References and recommended reading Papers of particular interest, published within the period of review, have been highlighted as:  of special interest  of outstanding interest 1.

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Ohashi K, Makino TT, Arikawa K: Floral colour change in the eyes of pollinators: testing possible constraints and correlated evolution. Funct Ecol 2015, 29:1144-1155. This study uses objective measures of flower reflectance to explore whether floral colour change is more apparent to evolutionary-relevant pollinators than to human observers. It also explores phylogenetic and biochemical constraints of floral colour change, and provides evidence that floral colour change might be particularly associated with certain pollinators (specifically bees).

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Niesenbaum RA, Patselas MG, Weiner SD: Does flower color change in Aster vimineus cue pollinators? Am Mid Nat 1999, 14:59-68. Current Opinion in Plant Biology 2016, 32:96–100

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Gori DF: Floral color change in Lupenus argenteus (Fabacae): why should plants advertise the location of unrewarding flowers to pollinators. Evolution 1989, 43:870-881.

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Ollerton J, Grace J, Smith K: Adaptive floral colour change in Erysimum scoparium (Brassicaceae) and pollinator behaviour of Anthophora alluadii on Tenerife (Hymenoptera: Apidae). Entomol Gen 2007, 29:252-268.

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Ida TY, Kudo G: Modification of bumblebee behaviour by floral color change and implications for pollen transfer in Weigela middendorffiana. Evol Ecol 2010, 24:671-684.

10. Gould KS: Nature’s Swiss Army knife: the diverse protective roles of anthocyanins in leaves. J Biomed Biotechnol 2004, 5:314-320. 11. Glover BJ, Martin C: Anthocyanins. Curr Biol 2012, 22:R147-R150. 12. Goyret J, Markwell PM, Raguso RA: Context- and scaledependent effects of floral CO2 on nectar foraging by Manduca sexta. PNAS 2008, 105:4565-4570. 13. Gori DF: Floral colour change in Lupinus argentus (Fabaceae): why should plants advertise the location of unrewarding flowers to pollinators? Evolution 1989, 43:870-881.

22. Pe´labon C, Hennet L, Strimbeck R, Johnson H, Armbruster WS: Blossom colour change after pollination provides carbon for  developing seeds. Funct Ecol 2015, 29:1137-1143. A valuable paper in encouraging consideration of consequences (and perhaps drivers) of floral colour change that are nothing to do with influencing pollinator behaviour; in this case exploration colour change is apparently driven by selection to increase local photosynthesis. 23. Jabbari SG, Davis SL, Carter EJ: Interaction between floral color change and gender transition in the protandrous weed Saponaria officinalis. Plant Species Biol 2013, 28:21-30. 24. Steyn WJ, Wand SJ, Holcroft DM, Jacobs G: Anthocyanins in vegetative tissues: a proposed unified function in photoprotection. New Phytol 2002, 155:349-361. 25. Ojeda DI, Santos-Guerra A, Oliva-Tejera F, Valido A, Xue X, Marrero A, Caujape´-Castells J, Cronk Q: Bird-pollinated Macaronesian Lotus (Leguminosae) evolved within a group of entomophilous ancestors with post-anthesis flower color change. Perspect Plant Ecol Evol Syst 2013, 15:193-204. 26. Ojeda DI, Valido A, Ferna´ndez de Castro AG, Ortega-Olivencia A, Fuertes-Aguilar J, Carvalho JA, Santos-Guera A: Pollinator shifts drive petal epidermal evolution on the Macaronesian Islands bird-flowered species. Biol Lett 2016, 12:20160022. 27. Rauscher MD: Evolutionary transitions in floral colour. Int J Plant Sci 2008, 169:7-21.

14. Suzuki MF, Ohasshi K: How does a floral colour-changing  species differ from its non-colour-changing congener? A comparison of trait combinations and their effects on pollination. Funct Ecol 2014, 28:549-560. This experimental study takes advantage of the patchy distribution of floral colour change within families to compare closely related species that naturally flourish in environments only one of which shows floral colour change. This system controls for a great many confounding factors but also avoids risk of unrealistic experimental manipulations to flower appearance. This study is also ground-breaking in focussing on the potential metabolic and ecological costs of floral colour change as much as on potential benefits.

28. Brito VL, Weynans K, Sazima M, Lunau K: Trees as huge flowers  and flowers as oversized floral guides: the role of floral color change and retention of old flowers in Tibouchina pulchra. Front Plant Sci 2015, 6:362. This is an important paper for exploration of the effects of floral colour change not just for individual flowers or for inflorescences, but at the whole-plant level that is most relevant to evolutionary ecology.

15. Ida TY, Kudo G: Floral color change in Weigelia middendorffiana (Caprifoliaceae): reduction of geitonogamous pollination by bumble bees. Am J Bot 2003, 90:1751-1757.

30. Kulahci IG, Dornhaus A, Papaj DR: Multimodal signals enhance decision making in foraging bumble-bees. Proc R Soc Lond B Biol Sci 2008, 275:797-802.

16. Sun SG, Liao K, Xia J, Guo YH: Floral colour change in Pedicularis monbeigiana (Orobanchaceae). Plant Syst Evol 2005, 255:77-85.

31. Katzenberger TD, Lunau K, Junker RR: Salience of multimodal flower cues manipulates initial responses and facilitates learning performance of bumblebees. Behav Ecol Sociobiol 2013, 67:1587-1599.

17. McGimpse VJ, Lord JM: In a world of white, flower colour  matters: a white–purple transition signals lack of reward in an alpine Euphrasia. Aust Ecol 2015, 40:701-708. This study takes advantage of the unusually high frequency of small white flowers amount the New Zealand alpine flora to explore selection for floral colour change in the wider context of the colour of other flowers that generalist pollinators are also likely to experience. This study also makes use of introduced Bombus bees as well as native syrphid pollinators, to explore the importance of co-evolution with pollinators to floral colour change.

29. Kudo G, Ishii HS, Hirabayashi Y, Ida TY: A test of the effect of floral color change on pollination effectiveness using artificial inflorescences visited by bumblebees. Oecologia 2007, 154:119-128.

32. Riffell JA, Alarco´n R: Multimodal floral signals and moth foraging decisions. PLOS ONE 2013, 8:e72809. 33. Hebets EA, Papaj DR: Complex signal function: developing a framework of testable hypotheses. Behav Ecol Sociobiol 2005, 57:197-214. 34. Bro-Jørgensen J: Dynamics of multiple signalling systems: animal communication in a world in flux. Trends Ecol Evol 2010, 25:292-300.

18. Chittka L, Niven J: Are bigger brains better? Curr Biol 2009, 19:R995-R1008.

35. Grotewold E: The genetics and biochemistry of floral pigments. Annu Rev Plant Biol 2006, 57:761-780.

19. Schaefer HM, Valido A, Jordano P: Birds see the true colours of fruits to live off the fat of the land. Proc R Soc B 2014, 281:20132516.

36. Galliot C, Stuurman J, Kuhlemeier C: The genetic dissection of floral pollination syndromes. Curr Opin Plant Biol 2006, 9:78-82.

20. Schiestl FP, Ayasse M: Post-pollination emission of a repellent compound in a sexually deceptive orchid: a new mechanism for maximising reproductive success? Oecologia 2001, 126:531-534. 21. Fusato Y, Itagaki T, Oguro M, Sakai M: Effect of change in floral  openness with floral age on floral display and reproduction in Gentiana. Acta Oecol 2015, 67:17-23. This paper encourages consideration of structural changes to the shape of flowers as an alternative or complimentary strategy to floral colour change.

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37. Zufall RA, Rausher MD: Genetic changes associated with floral  adaptation restrict future evolutionary potential. Nature 2004, 428:847-850. This is an important paper showing that very few genetic changes can lead to the inactivation of an anthocyanin pigment pathway leading to changes in floral colour. 38. Hoballah ME, Gu¨bitz T, Stuurman J, Broger L, Barone M et al.: Single gene-mediated shift in pollinator attraction in Petunia. Plant Cell 2007, 19:779-790.

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