Nectar spurs, hawkmoths, and diversification in flowering plants

Featured photo by Kelly Ricetti

Darwin’s Orchid and Wallace’s Sphinx Moth

In the early 1860’s, Charles Darwin was working on a book detailing the various ways in which orchids are pollinated. Just shy of four months before its publication, on January 25, 1862, Darwin received a curious package, the contents of which would have resounding implications for his theory of evolution. Inside were several orchids, sent no doubt to help assist in his current literary endeavor, by a man named James Bateman, who specialized in growing them. Upon examining the specimens, Darwin’s excitement was immediately piqued by an orchid with extremely long nectar spurs. He was so excited that he wrote a letter to his closest friend, Joseph Dalton Hooker, the same day, exclaiming, “I have just received such a box full from Mr. Bateman with the astounding Angraecum sesquipedale [sic] with a nectary a foot long. Good Heavens, what insect can suck it” (Darwin, 1862).

The answer to that question would remain a mystery for another 41 years, but that didn’t stop Darwin from making a prediction as to what it might be and look like. Moths often have a long, slender proboscis, which they use to drink out of flower nectaries. In the process, the moths will come into contact with the pollen-laden anthers of the flowers, thus acting as pollinators when they venture to the next flower in search of food. But the longer a moth’s tongue, the less likely its head will touch the anthers. The flowers must therefore produce increasingly long nectar spurs to entice the moths to come closer or face extinction, giving rise to an evolutionary arms race. In Darwin’s own words,

“As certain moths of Madagascar became larger through natural selection in relation to their general conditions of life…or as the proboscis alone was lengthened to obtain honey from the Angræcum and other deep tubular flowers, those individual plants of the Angræcum which had the longest nectaries…and which, consequently, compelled the moths to insert their probosces up to the very base, would be fertilised. These plants would yield most seed, and the seedlings would generally inherit longer nectaries; and so it would be in successive generations of the plant and moth. Thus it would appear that there has been a race in gaining length between the nectary of the Angræcum and the proboscis of certain moths…” (Darwin, 1904: 165).

 

This would become one of Darwin’s first postulations on what later became known as coevolution, and which Darwin would go on to describe more fully in the Origin of Species. Darwin had predicted the existence of an unknown species based solely on the length of a nectar spur, but it would be several decades before his prediction would be verified.

In the meantime, Darwin had several critics, and one such opponent, George Campbell, in arguing for special creation, seized upon a vague phrase written by Darwin that stated, in regard to his theory of nectar spur elongation, “we can thus partially understand how this astonishing nectary was produced.” Campbell argued semantics, maintaining that Darwin had merely procured a partial explanation, with the implied assumption that only God could have given rise to such a complicated relationship between flower and moth (Campbell, 1884). But Alfred Russel Wallace, co-discoverer of the theory of evolution and one of Darwin’s staunchest defenders, wrote a lengthy response to several of Campbell’s criticisms, including his comments on nectar spurs. The result was an in-depth description of how both the orchid and moth, still as yet undiscovered, might have coevolved, to which he appended an illustration depicting what the moth may have looked like (Wallace, 1867).

wallacesesquipedale

41 years after the first edition of Darwin’s orchid book, researchers claimed they had found the fabled sphinx moth, which has a probiscus up to 15cm long, naming it Xanthopan morgani praedicta, referencing the prediction of its existence, although since the authors mention only Wallace in their explanation of the nomenclature, it’s generally assumed that the name was in honor of his lengthy description and illustration of the moth (Rothschild and Jordan, 1903). But even then, researchers had never directly observed the moth pollinating specimens of Angraecum sesquipedale. That would end up having to wait for almost a hundred years, when the first account of such an occurrence was published in 1997 (Wasserthal).

Rapid Radiation in Ranunculaceae

In July of 1879, Darwin famously wrote to Joseph Hooker, “The rapid development as far as we can judge of all the higher plants within recent geological times is an abominable mystery” (Darwin and Seeward, 1903). Just what did he mean by this cryptic statement? The truth was that the rapid origin of angiosperms, at the time, seemed to threaten Darwin’s entire theory of evolution. Darwin adhered to the principle natura non facit saltum, nature does not make a leap, meaning that any evolution through natural selection occurs very slowly and gradually, which he wrote about at length in the last chapter of Origin of Species (1859). And yet, here was direct evidence to the contrary. In the fossil record, angiosperms appear suddenly in the Cretaceous, and in the geologic blink of an eye became the dominant group of plants on the planet, comprising 96% of vascular plant diversity (Judd et al. 2002).

Darwin never really came to a firm conclusion as to how angiosperms diversified so quickly, although he was given part of the answer by a French paleontologist named Gaston de Saporta, who attested that the mechanism underlying the diversification of angiosperms was their coevolution with insects (Friedman, 2009). Just recently, it’s been discovered that the first angiosperms are also older than previously suspected, with fossils of Archaefructus and Montsechia being some 130 million years old, with a potential origin predating that by several million years (Sun et al., 1998; Krassilov, 2011). However, the theory of coevolution with insects remains the most widely accepted to date to explain angiosperm diversification. But it turns out that coevolution can lead to even higher rates of diversification in some circumstances, and the length of nectar spurs in flowering plants can be a major contributing factor.

One of the best known examples is that of columbines, in the buttercup family (Hodges and Arnold, 1995). Common favorites in the garden, columbines are known for their pendulous, bell-shaped flowers that display an astonishing variety of color. They possess nectar spurs positioned directly behind a mass of protruding anthers, making it virtually impossible for their pollinators to obtain the carefully sequestered nectar without also inadvertently collecting a fair share of pollen. The 70 or so species of columbines have very little amounts of sequence divergence between them, meaning they all evolved relatively recently and quickly compared to their close relatives. The cause of this rapid radiation is the varying lengths of their nectar spurs, which range from 1 to 15cm (Puzey et al., 2011).

There are two distinct trends that can potentially be observed in this group (Whittall and Hodges, 2007). When columbines first evolved, evidence suggests that they were all initially pollinated by bumble-bees, which have short proboscises. Those that are still pollinated by bees today have correspondingly short nectar spurs, most at around 1cm in length. But as new species evolved, there was a switch to hummingbird pollinators, whose tongues are slightly longer than that of bees. In order to ensure that their new pollinators didn’t make off with the nectar without transporting pollen as well, the nectar spurs of these flowers increased in length accordingly. Later on, there was yet another switch, this time from hummingbirds to hawkmoths, which have the longest tongues of all, requiring that the flowers they pollinated possessed nectar spurs of appropriate length. It’s in the last group that we see a large amount of variation in the length of nectar spurs, from around 3cm to 15cm, likely indicating that Darwin’s arms race is occurring there between hawkmoth and flower. Each time a pollinator shift occurred (and there were several shifts, including at least one reversal), flowers with differing spur lengths became genetically isolated, since their pollinators would only visit the flowers with spurs that corresponded to their tongue length, promoting rapid speciation.

Aquilegia vulgaris, which is pollinated by bumble-bees.
Aquilegia vulgaris, which is pollinated by bumble-bees.
Aquilegia formosa, which is pollinated by hummingbirds
Aquilegia formosa, which is pollinated by hummingbirds
Aquilegia chrysantha, which is pollinated by hawkmoths
Aquilegia chrysantha, which is pollinated by hawkmoths

This type of accelerated diversification is not peculiar to just columbines, but can be seen in several groups of plants with nectar spurs, including bleeding hearts (Fumariaceae), bladderworts (Lentibulariaceae), and nasturtiums (Tropaeolaceae) (Hodges and Arnold, 1997), as well as just about any organism with a trait that promotes genetic isolation, such as birds with complex mating rituals and a variety of bioluminescent invertebrates (squid, ostracods, etc…) (Ellis and Oakley, 2016). In plants, they help to partially explain how angiosperms were able to evolve so quickly, leading not only to the evolution of several orders of insects, but to our own existence as well.

References

Campbell GJD. (8th Duke of Argyll). 1884. Reign of law. New York: A. L. Burt.

Darwin, C. 1859. On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life, 1st ed. John Murray, London, UK.

Darwin CR. 1862b. Letter 3411-Darwin, C. R., to Hooker, J. D, 25 January 1862. Available at: http://www.darwinproject.ac.uk/ entry-3411

Darwin, F., Seeward, A.C., 1903. More Letters of Charles Darwin: a Record of his Work in a Series of Hitherto Unpublished Papers, Vol. II. John Murray, London.

Darwin CR. 1904. The various contrivances by which orchids are fertilised by insects. 7th impression of the 2nd edition. London: John Murray. The first printing of the second edition was in 1877.

Ellis, E. A., & Oakley, T. H. (2016). High rates of species accumulation in animals with bioluminescent courtship displays. Current Biology, 26: 1916-1921.

Friedman, W. E. (2009). The meaning of Darwin’s “abominable mystery”. American Journal of Botany, 96: 5-21.

Hodges, S. A., & Arnold, M. L. (1995). Spurring plant diversification: are floral nectar spurs a key innovation? Proceedings of the Royal Society of London B: Biological Sciences, 262: 343-348.

Judd W.S., Campbell, C.S., Kellogg, E.A., Stevens, P.F., and Donoghue, M.J. (2002) Plant Systematics: A Phylogenetic Approach, Second Edition. Sinauer Associates, Sunderland.

Krassilov, V. A. (2011). On Montsechia, an angiospermoid plant from the Lower Cretaceous of Las Hoyas, Spain: new data and interpretations. Acta Palaeobot, 51: 181-205.

Puzey, J. R., Gerbode, S. J., Hodges, S. A., Kramer, E. M., & Mahadevan, L. (2011). Evolution of spur-length diversity in Aquilegia petals is achieved solely through cell-shape anisotropy. Proceedings of the Royal Society of London B: Biological Sciences, rspb20111873.

Rothschild LW, Jordan K. 1903. A revision of the lepi- dopterous family Sphingidae. Novitates Zoologicae 9 (Supplement), cxxxv plus 972 pp. plus 67 plates (Xanthopan is on pages 5, 28, 30–33, 817).

Sun, G., Dilcher, D. L., Zheng, S., & Zhou, Z. (1998). In search of the first flower: a Jurassic angiosperm, Archaefructus, from northeast China. Science, 282: 1692-1695.

Wallace AR. 1867. Creation by law. The Quarterly Journal of Science 4: 471–488.

Wasserthal LT. 1997. The pollinators of the Malagasy star orchids Angraecum sesquipedale, A. sororium, and A. com- pactum and the evolution of extremely long spurs by polli- nator shift. Botanica Acta 110: 343–359.

Whittall, J. B., & Hodges, S. A. (2007). Pollinator shifts drive increasingly long nectar spurs in columbine flowers. Nature, 447: 706-709.

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