Introduction to the Red-Flower Project

Plants are often overlooked as the background against which all other life is performed.  And yet, the sessile nature of the plant community requires that these organisms act most dynamically, adapting complex and changing responses to their environment.  Perhaps the most convincing evidence for this is the diversity and abundance of flowering plants, which host incredible variations in both floral display and the animal interactions that they elicit.

As biologists,  we are interested in understanding how the relationships between flowers and pollinators first evolved, and how these interactions continue to drive the evolution of floral traits.  We wonder how opposing pressures to prevent herbivory and also ensure pollination can combine to influence floral characteristics, and we question whether similar pressures and pollination strategies can produce convergent evolution of floral traits.

This project attempts to get at many of these questions by studying a group of unrelated flowers that share in common similar floral traits and a long biological history.  This group is characterized by having red flowers that bloom in early spring and emit unusual, musky odors.  Importantly, the flowers that we study are unlike most of their closest relatives and co-blooming plants, which bear white flowers and emit sweet odors.  By exploring the reproductive strategies of this red-flower guild, we hope to begin answering how flower characteristics evolve as functional responses to environmental pressures.  From here, we might begin to understand the context in which the first pollination systems evolved.

Living Fossils

What is a living fossil?

We use the term "living fossil" to describe a lineage that have survived, relatively unchanged, for millions of years.  Most of these organisms have endured mass extinction events and exist today as living relics of ancient life.  These "living fossils" are important because they can provide clues about earth's history.  Studying these ancient organisms also can help us to understand how modern species first evolved and to recognize patterns of evolution that continue to influence our changing world.
 

Image: Wong Maye-E / Associated Press 

The nautilus (top left) is the only living member of an otherwise extinct group of cephalopods.  Below, fossil evidence demonstrates that extinct ammonites, close relatives of the nautilus, were once abundant marine animals.

With their hinged exoskeleton and hardened tail (telson), the curious-looking horseshoe crab appears the very epitome of a living fossil.  In fact, these organisms belong to a primitive group of marine arthropods.  Horseshoe crabs are the only of their kind to have survived the mass extinction that brought about the end of the dinosaurs, as well as half the planet's marine invertebrates.

Image: Great Lakes Image Collection

Image: University of Chicago Medical Center

Dating back at least 360 million years, the eel-like lamprey is the most primitive of all vertebrates.  Unlike modern fish, the lamprey is a jawless parasite that lacks scales and paired fins.  Lampreys are of interest to scientists, who hope to understand how these ancestral fish fit into the evolutionary scheme that gave rise to the diversity of modern vertebrates.

Image: M McKelvey/ P Rismiller

The echidna (bottom right) and platypus (top right) are the only living representatives of the group of egg-laying mammals called monotremes.  These organisms are believed to have diverged from the mammalian lineage some 150 million years ago, and are distinct from two mammalian sister groups, the marsupials and the placental mammals.  Monotremes are important for answering fundamental questions about the common ancestor to these three distinct mammalian groups.

                                                                                                           

Plants Can Be Living Fossils Too

Relictual plant species are also important for describing earth's biological history and the evolutionary trends shaping the planet's future.

Image: John Cancalosi/Alamy

For example, the horsetail (Equisetum) is a vascular plant that was once abundant during the Paleozoic era.  This species is a fern belonging to the group, Pteridophyta, which reproduce by way of spores rather than seeds.  Today's horsetails are small understory plants, though millions of years ago, this diverse group included tree-like species that measured 30 meters tall.


The ginko tree is another living relic of a once prolific group of gynosperms called the Ginkgoales.  Today, Ginkgo biloba is the only remaining species from this group.
 

Ancient Angiosperms

The evolution of reproductive systems in plants, and particularly, the emergence of flowers, has had reciprocal effects on the diversification and proliferation of all other life on this planet.


Today, angiosperms are widespread, diverse, and hugely important to the global ecosystem.  Their success can be largely attributed to the mutalistic relationships that flowers have evolved with their animal pollinators, who facilitate sexual reproduction, and thus ensure genetic diversity in these plants.



Although the origin of flowering plants are still poorly understood, both phylogenetic and fossil evidence suggest that water lilies are among the most ancient groups of angiosperms. 

Surprisingly little is understood about the origins of flowering plants.  Without the ability to rewind history, scientists are forced to use creative methods for resolving questions like,


How did the first flowers evolve?  What pollinated these flowers?  What motivated these pollinators? 

One strategy hinges on the assumption that ancient angiosperm species retain qualities of the earliest flowering plants.  By studying these flowers and their modern pollination strategies, we might make inferences about the first adaptations for pollination in angiosperms.

Predicting what the first angiosperm pollination systems looked like involves answering a number of questions.

1. Were the first flowers pollinated by wind/water or by animals?          
Pairing clues from ancient floral morphology with our knowledge of modern wind and animal pollinated species helps us to answer this question.  Based on this information, scientists have determined that the first flowers were almost certainly animal pollinated.
  

2. What kind of potential pollinators existed before the first angiosperms evolved? 

We know from studying the fossil record that insects evolved before the first flowering plants.  Many of the insect orders that, today, are major pollinators of modern flowers already existed before angiosperms first arrived.  These include beetles (Coleoptera), flies (Diptera), wasps (Hymenoptera), moths and butterflies (Lepidoptera), and to some extent, thrips (Thysanoptera).  The feeding structures on these animals tell us that the earliest insects fed on carrion, detritus, and plant tissue.  (Damaged fossilized plant tissue supports this theory).  This strongly suggests that many of these insects were already adapted to search for food at non-flowering plants.
   

Using fossil evidence for support, some scientists propose that insects, such as scorpionflies, may have been early pollinators of gymnosperms.  If true, this would indicate that insects were already pollinating plants before the first flowers ever appeared.


3.  Prior to the evolution of flowers, did any plant species involve animals in their pollination strategies?

Image: New York Botanical Garden

Yes.  Although modern gymnosperms are almost entirely wind-pollinated, we know that at least some of their ancient relatives used insects for pollination.  For example, cycads are a living fossil representative of the first group of gymnosperms.  Unlike many of their extant relatives, we know that modern cycads are morphologically restricted to animal-pollination.  These plants use beetles, thrips, and moths to pollinate their reproductive cones.


4.  How did the first flowers entice insects to visit them?
         
We are still answering this question!  As stated, insects were adapted to feed on plant tissue before angiosperms first evolved.  This means that insects were already visiting plants in search of food.  But how did flowering species persuade these insects to visit their novel reproductive structures, while also preventing herbivory?


One hypothesis is that the plants used what they already had.  Before flowers evolved, plants already possessed the chemical equipment to defend against herbivory and disease.  It is postulated that primitive floral odors were simply derivatives of these defensive volatile chemicals.  In fact, we already know that these two functional classes of compounds share a similar biosynthetic pathway.


It is possible that some insects may have developed a tolerance for certain plant chemicals.  Instead of acting as a deterrent, the plant volatiles could have evolved to signal such things as a food source or mating site for those insects.  Furthermore, some evidence suggests that odor was the first floral characteristic to have evolved as a pollinator attracting in angiosperms.  Flower color and morphology may have become increasingly important as these plant-animal mutualisms proliferated and specialized.  


The arching theme of this study and of pollination biology, in general, is asking,

What modes of communication do plants use to signal to pollinators?

Flowering plants invest immense resources into their floral structures, in order to ensure that their genes are distributed.  It is consequently important that plants successfully attract pollinators to their flowers.

Floral morphology, color, and odor are the main cues used by flowering plants to advertise their rewards.  Variations in these traits and in the combinations in which they are used by flowers is dependent, primarily, on which pollinators these plants are selected to attract.  Understanding innate pollinator preferences to these modes of floral communication helps us to predict the evolving dynamics of flowers and their pollinators. 


 

Pollination Syndromes

Often, when unrelated angiosperm species utilize the same groups of animals for pollination, their flowers will exhibit similar characteristics.  For example, moth-pollinated flowers tend to be white colored with long nectar tubes.  They typically open in the evening, exhibiting strong, sweet smelling odors and offering relatively large amounts of nectar.

Image: Charles Hedgcock

The mutualistic relationship between an angiosperm and its pollinators presupposes that selective pressures exhibited by the pollinators will choose for floral traits that favor the most effective and abundant pollinators.  Consequently, flowers pollinated primarily by moths open in the evening because moths are nocturnal feeders.  Odor tends to be potent in these flowers because moth orientation in the low light levels of the evening relies more heavily on non-visual cues.  Long nectar tubes are also favored in these flowers because they allow the plants to reserve their rewards for only able pollinators, like moths, who can reach the nectar source with a lengthy proboscis.  And because metabolic rate is astoundingly high in these insects, moth-pollinated flowers offer plenty of energy-rich nectar to compensate for the costs of flight. 

Image: Jiao-Kun Li and Shuang-Quan Huang

When flowers rely on a specific group of animals for pollination, we refer to this as a specialized pollinator mutualism.  Often in these plants, floral traits are indicative of the specific mutualism, in which case these collective floral characteristics are termed a pollination syndrome.

In contrast, some flowers do not have specialized relationships with particular pollinators.  These species rely on a group of generalized insects to carry out their pollination activities.  In such circumstances, floral traits are selected for not by a single dominant pollinator, but by the combined influence of all the acting pollinators.  Floral traits in these species consequently do not favor a single type of pollinator, and cannot be characterized by a "pollination syndrome."  When flowers are pollinated by a broad group of insects, we call this a generalized pollination system.

For example, in the Asian sacred lotus flower (right), scientists observed bees (A,B), beetles, (C,D), flies (E), and thrips (F) all visiting the same flowers. 

Red Flower Guild

Did the first angiosperms have specialized or generalized pollinator mutualisms?

Some of the oldest extant angiosperm species display floral characteristics that have biologists confused.  These plants produce red flowers that bloom early in the spring and exude musky, unpleasant odors.  In contrast, most co-blooming spring perennials have light-colored flowers with sweet odors.  What is more surprising is that these unusual red-flowered relict species might be exhibiting a form of specialization.  By studying these flowers, we hope to determine whether they demonstrate a novel pollination syndrome, of if their unusual combination of floral characteristics evolved to attract a general group of insects.  From here, potential inferences may be allowed about the origins of angiosperm-pollinator mutualisms.

Check it out!

Three of the ancient red-flowered species in our study can be found growing in the Georgia Southern Botanical Garden.

Florida anise (Illicium floridanum) is an evergreen shrub that grows in the understory of wooded ravines from the Florida panhandle up through Louisiana.  Fossil records give evidence for the long history of this species, which has existed for some 40+ million years, and was once far more abundant throughout Asia and North America.  While the leaves of I. floridanum smell strongly of anise, its deep red flowers, which bloom in early spring, emit odors akin to fish.  Very little is known about the pollination of this ancient species.


Calycanthus floridus is a woody evergreen shrub native to eastern North America.  It ranges from Florida north to New York, where it thrives in the understory of moist forests.  Similar to the genus, Illicium, the leaves of this plant smell strongly medicinal, and for this reason, C. floridus is commonly referred to as sweet shrub or Carolina allspice.




Asimina triloba, the common paw paw, represents the northernmost range of a group of tropical angiosperms (Annonaceae).  This species grows as an understory shrub from Illinois to New York,  south to Florida and west to Texas.  Its flowers bloom in early spring and produce a large, edible fruit which ripens in the fall and is known for its custard-like texture. 




Each of the red-flowered species that we study has relatives in the same genus which bear white, sweet smelling flowers and tend to bloom in the late spring.  We use these white-flowered species for comparison, with the hypothesis that there is a functional significance for the difference in color, odor, and phenology between white and red-flowered species.  Based on our understanding of pollinator preferences for floral color and odor, we expect these red flowers to attract different insect pollinators than their white-flowered relatives.  If true, the evolution of these floral patterns may be a mechanism for carving a functional niche in the pollination scheme.

From top, Illicium floridanum and its white-flowered relative, Illicium anisatum, can both be found at the Georgia Southern Botanical Garden.  Also look for Calycanthus floridus and its white-flowered counterpart, Sinocalycanthus chinensis (middle row).  Lastly, the red-flowered Asimina triloba can be found among the specimen at the G.S. Botanical Garden, but the white-flowered Asimina reticulata is restricted to regions of central and southern Florida.

The Common Garden Experiment

One complication of a study involving ancient flowers is the spatial separation of our species.  Ideally, we would study natural populations of co-occurring red and white flowered relatives.  However, the flower lineages that we study have persisted through millions of years of global change, including climate shift, continental drift, and habitat fragmentation, which have altered the original environments.  Though the red and white flowered varieties of each genus most likely overlapped in habitat, at one time, they have since become isolated by change.

Spatial segregation of red and white flowered relatives makes it difficult to answer questions like, "Do stinky red flowers attract different pollinators than sweet-smelling white flowers?"  because the environmental conditions of these two flowers are not comparable.  One solution for this problem is to conduct a common garden experiment, where populations of each species are grown together in a shared garden space.  This type of experiment resolves environmental disparities that might contribute to variance in results and observations.  With a common garden, we can be confident that any differences in pollination or floral phenology are due to a divergence in floral strategy, rather than a product of environmental incongruities. 

The Georgia Southern Botanical Gardens offer a unique opportunity to observe a common garden of living fossils!  A white flowered relative of Carolina allspice, Sinocalycanthus chinensis, is an endangered species endemic to regions of China.  Similarly, Illicium anisatum, the white flowered Japanese star anise, does not occur naturally outside of Japan and Taiwan.  With the exception of botanical collections, these species cannot be found in the United States, making the GSBG a rare place to study the pollination strategies of these white flowers. 

Related Literature

Living Fossils

Janvier, Philippe.  (2006) Palaeontology: Modern look for ancient lamprey.  Nature 443, 921-924.  http://www.nature.com/nature/journal/v443/n7114/full/443921a.html 

Other Fish in the Sea (website).  http://www.pbs.org/wgbh/nova/nature/other-fish-sea.html

The Evolution of Pollination

Grimaldi, David.  (1999) The co-radiations of pollinating insects and angiosperms in the Cretaceous.  Annals of the Missouri Botanical Garden 86(2), 373-406

Pellmyr, O. and L. Thien.  (1986) Insect reproduction and floral fragrance: Keys to the evolution of angiosperms?  Taxon 35, 76-85

Ren, D. et al.  (2009) A probable pollination mode before angiosperms: Eurasian, long-proboscid scorpionflies.  Science 326, 840-847


Pollination Syndromes


Li, J.-K. and S.-Q. Huang.  (2009) Effective pollinators of Asian sacred lotus (Nelumbo nucifera): contemporary pollinators may not reflect the historical pollination syndrome. Annals of Botany 104(5): 845-851

Waser, N.M. et al.  (1996) Generalization in pollination systems, and why it matters.  Ecology 77:1043–1060.


Red Flower Guild


Thien, L.B., D.A. White, and L.Y. Yatsu.  (1983) The reproductive biology of a relict- Illicium floridanum (Ellis).  Amer. J. Bot. 70(5): 719-727


Wilson, M.F., and D.W. Schemske.  (1980) Pollinator limitation, fruit production, and floral display in pawpaw (Asimina triloba).  Bulletin of the Torrey Botanical Club 107(3): 401-408