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the authors state, however, regardless of the exact 3 Crepet, W.L. and Niklas, K.J. (2009) Darwin’s second ‘‘abominable

mystery’’: Why are there so many angiosperm species? Am. J. Bot. 96,

mechanisms involved, the slower evolution of reproductive

366–381

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4 Smith, A.R. (1972) Comparison of fern and flowering plant distributions

plants may account for the relative paucity of species, in with some evolutionary interpretations for ferns. Biotropica 4, 4–9

part, by enforcing a ‘low birth rate of new species.’ The 5 Ackerman, J.D. (2000) Abiotic pollen and pollination: ecological,

functional, and evolutionary perspectives. Plant Syst. Evol. 222,

relatively high rates of gene flow that would follow from

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Concluding remarks

8 Fraser-Jenkins, C.R. (2008) Taxonomic revision of three hundred

The impressive species richness of the flowering plants is Indian subcontinental pteridophytes with a revised census-list: a

undoubtedly due to many interacting factors that vary in new picture of fern- and nomenclature in the Indian

their effects across lineages. By contrast, though, could the subcontinent. Bishen Singh Mahendra Pal Singh, Dehra Dun, India

9 Tsutsumi, C. et al. (2011) A new allotetraploid species of Osmunda

lower speciation rates of ferns and other abiotically

(Osmundaceae). Syst. Bot. 36, 836–844

dispersed, non-flowering land plants primarily be driven

10 Schneider, H. et al. (2015) Are the genomes of royal ferns really frozen

by high rates of gene flow? in time? Evidence for coinciding genome stability and limited

evolvability in the royal ferns. New Phytol. http://dx.doi.org/10.1111/

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1 Stebbins, G.L. (1981) Why are there so many species of flowering 11 Bomfleur, B. et al. (2014) Fossilized nuclei and chromosomes reveal

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where are they, and at what rate are they going extinct? Ann. Missouri 12 Ellstrand, N. (2014) Is gene flow the most important evolutionary force

Bot. Gard. 100, 170–176 in plants? Am J. Bot. 101, 737–753

Active pollinator choice by ‘fits the bill’

Judith L. Bronstein and Sarah K. Richman

Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721 USA

A new study documents that a tropical plant only repro- er, researchers have focused on how evolved traits, such as

duces when pollen has been deposited by a visitor corolla length and nectar chemistry, allow plants to at-

capable of extracting nectar from its deep flowers. Large, tract and reward the best pollinators. Such mechanisms

long-billed generally carry greater quan- are far from perfect, though. Plants lose much of their

tities of, and more genetically diverse, pollen. Thus, nectar to visitors that deposit low-quality pollen (or none

plants can exert more active partner choice than previ- at all).

ously considered possible. However, a new study by Matthew Betts, Adam Hadley,

and John Kress[3] suggests that plants may be more able to

A inserting its long bill into a red, tubular selectively associate with good pollinators than has previ-

flower is an iconic image of pollination. Although this ously been thought possible.

image leads one to think about trait-matching and pair- Heliconia tortuosa Griggs (Heliconiaceae) possesses

wise coevolution, as a rule each pollinator species visits long, tubular, curved, yellow flowers which are held

more than one plant species, which in turn is visited by within bright red bracts. In Costa Rica, they are visited

more than one pollinator [1]. On each side of the mutual- by a suite of hummingbird species that vary considerably

ism, some partners confer higher benefits than others. in traits likely to affect their quality as pollinators. Betts

How can plants and animals filter out the worst partners, et al. started their study of H. tortuosa with a standard

and consistently associate with the best? Pollinators com- experiment in pollination biology: they compared pollen-

monly learn to discriminate among plants, choosing those tube formation between flowers exposed to humming-

likely to offer the most nectar [2]. By contrast, plants have birds in nature, and flowers protected from humming-

been thought incapable of assessing pollinator quality and birds but pollinated by hand. Perplexingly, flowers given

then acting instantaneously upon this information. Rath- an excess of hand-deposited pollen initiated fewer pollen

tubes, not more. This effect, however, disappeared when

Corresponding author: Bronstein, J.L. ([email protected])

Keywords: coevolution; hummingbird; partner choice; pollination; reproduction; the researchers also drained the nectar during the hand-

mutualism. pollination treatment. Betts et al. formulated a clever

1360-1385/ explanation for these odd results. They conjectured that

ß 2015 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tplants.2015.04.010

the plant will only invest in reproduction if some type of

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Spotlights Trends in Plant Science July 2015, Vol. 20, No. 7

signal is sent by the flower visitors, e.g., the pollen was somewhat surprising from the standpoint of mutualism

deposited by a visitor capable of extracting the deep theory. The net effect of any mutualist is the benefit of its

nectar. By doing so, the plant would increase the likeli- effects minus the costs involved in attracting and reward-

hood that its seeds will be fathered by the best mates. ing it. Hence, selection should favor partners whose ben-

Large, long-billed species often fly long distances among efits can be obtained at the lowest cost [8]. However, in this

flowers of a single species (‘traplining’); by contrast, case, the best mutualists are intrinsically the most ener-

smaller short-billed hummingbirds establish territories, getically demanding ones (because they are large and fly

restricting their foraging to fewer plants. Trapliners long distances). That is, to receive a high benefit, H.

generally carry more genetically diverse pollen from tortuosa may be forced to make a high investment. The

numerous parents and for this reason are considered present study serves to emphasize that costs and benefits

superior pollinators. can act as constraints upon each other.

To test their hypothesis, six hummingbird and one Questions remain about the physiological mechanism

butterfly species were allowed to make single visits to by which H. tortuosa can discriminate among floral visi-

flowers on whose stigmas the researchers had placed pol- tors. Betts et al. argue that nectar removal, in conjunction

len; pollen tube numbers were then compared to flowers with pollen deposition, is all that is needed to stimulate

that had been hand-pollinated only. Two large traplining pollen tube formation. These results do not indicate how

hummingbirds with long, curved bills, the violet sablewing this happens – for example, whether plants are able to

and , removed significantly more nectar than identify high quality pollen on the stigmatic surface, or

the other visitors. Their visits also led to significantly more whether low quality pollen is selectively inhibited from

pollen tubes. The authors concluded that nectar removal germinating. This distinction is particularly important,

provides a cue for H. tortuosa to recognize floral visitors because, in nature, individual H. tortuosa flowers likely

and, in the authors’ words, to ‘turn on reproductively.’ receive multiple visits, possibly by more than one species of

Betts et al.’s study demonstrates clearly that appar- visitor. Quantifying pollen discrimination in response to

ently generalized interactions can hide cryptic speciali- pollen deposition by multiple visitors would seem to be a

zation. The authors use their results to suggest that critical follow-up study.

pairwise coevolution may be more prevalent in multispe- Finally, we note that this intriguing work rests solidly

cies associations than many researchers had assumed on a strong foundation of understanding the natural

earlier. history of the system. It would have been easy for Betts

We would like to stress two additional broad implica- and his colleagues to have dismissed their initial, puzzling

tions of this study. First, plants apparently possess much results as an experimental artifact. Instead, building on a

more active abilities to discriminate among partners than deep understanding of pollination biology, hummingbird

previously believed. (We note that the researchers have behavior, and tropical ecology and exhibiting a keen eye

not yet demonstrated that the pollen deposited by the for a clever and revealing experiment, they have offered

violet sablewing and green hermit is indeed of higher us new insight into an unsuspected aspect of plant bio-

quality, although it is a reasonable conjecture.) Recent logy. So many equally exciting discoveries remain to be

research has uncovered diverse but cryptic adaptations discovered.

that allow plants to deliver rewards only to the subset of

visitor species that, on average, are good mutualists, not References

only in pollination mutualisms [4] but in seed dispersal 1 Va´zquez, D. et al. (2012) The strength of plant-pollinator interactions.

[5] and ant protection [6] mutualisms as well. In the Ecology 93, 719–725

2 Goulson, D. (1999) Foraging strategies of insects for gathering nectar

present case, however, something different is going on:

and pollen, and implications for plant ecology and evolution. Perspect.

by actively discriminating among floral mutualists, H.

Plant Ecol. Evol. Syst. 2, 185–209

tortuosa is also selecting among mates. A clear parallel is 3 Betts, M.G. et al. (2015) Pollinator recognition by a keystone tropical

found in insects, in which females of some species exert plant. Proc. Natl. Acad. Sci. U.S.A. 112, 3433–3438

4 Pellmyr, O. and Huth, C.J. (1994) Evolutionary stability of mutualism

‘cryptic choice’ and selectively fertilize their eggs with the

between yuccas and yucca moths. Nature 372, 257–260

best sperm they receive [7]. An exciting challenge is to

5 Tewksbury, J.J. and Nabhan, G.P. (2001) Directed deterrence by

develop hypotheses that predict when similar discrimi-

capsaicin in chillies. Nature 412, 403–404

natory mechanisms will evolve in plants. A first step, 6 Orona-Tamayo, D. et al. (2013) Exclusive rewards in mutualisms:

certainly, is to look for it in Heliconia species other than ant proteases and plant protease inhibitors create a lock-key system

to protect Acacia food bodies from exploitation. Mol. Ecol. 22,

H. tortuosa, using the simple but clever experimental

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protocol presented in this paper.

7 Lu¨ pold, S. et al. (2013) Female mediation of competitive fertilization

A second implication emerges from the observation that

success in Drosophila melanogaster. Proc. Natl. Acad. Sci. U.S.A. 110,

in this study, the most effective pollinator species were 10693–10698

those visitors that removed the most nectar. This result is 8 Bronstein, J.L. (2001) The costs of mutualism. Am. Zool. 41, 127–141

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