Signal Dishonesty
Flowers are so dazzlingly diverse in form and function that there exists no one Platonic ideal of a flower. Despite the powerful aesthetic and emotional appeal that flowers have on the human psyche, most flowers are engaged in the commerce of offering energetic or nutritious rewards in exchange for the pollination services of animal visitors. In this light, I have described flowers as sensory billboards, advertising their nectar or pollen commodities with colors, patterns, scents and other stimuli that pollinators find attractive or can easily learn in association with floral rewards.
Flowers are so dazzlingly diverse in form and function that there exists no one Platonic ideal of a flower. Despite the powerful aesthetic and emotional appeal that flowers have on the human psyche, most flowers are engaged in the commerce of offering energetic or nutritious rewards in exchange for the pollination services of animal visitors. In this light, I have described flowers as sensory billboards, advertising their nectar or pollen commodities with colors, patterns, scents and other stimuli that pollinators find attractive or can easily learn in association with floral rewards.
Nevertheless, a surprisingly large number of flowering plants engage in mimicry or deception, in which their floral organs look, smell or even feel like a rewarding flower (food deception), a female insect (sexual deception) or decaying organic matter (brood site deception). My students and I have been intrigued by the gruesome examples of brood site deception, which include some of the world’s largest and most malodorous flowers (titan arum, giant rafflesia, giant stapelia), whose evolutionary histories boggle the imagination. The signals mediating such floral fraudulence can be so effective that blowflies will lay eggs into carrion flowers, representing direct fitness consequences for their "cognitive misclassification" of flowers as dead animals. We are equally interested in the HOW questions (How do floral tissues mimic sites of decay? How is each act of the masquerade (scent emission, heat production, floral movement) regulated? How do plant genomes accommodate such unusual developmental and biosynthetic shifts?) and the WHY questions (What selective forces would compel evolutionary shifts from rewarding flowers to deceptive ones? What intermediate steps might accompany such shifts?).
[Left, Prof. Raguso with "Wee Stinky", one of two Amorphophallus titanum plants that has bloomed semi-regularly at Cornell since 2010, thanks to Paul Cooper. Vacuum pumps and SPME fibers are suspended on the strings, collecting volatiles during the time course of blooming]
[Left, Prof. Raguso with "Wee Stinky", one of two Amorphophallus titanum plants that has bloomed semi-regularly at Cornell since 2010, thanks to Paul Cooper. Vacuum pumps and SPME fibers are suspended on the strings, collecting volatiles during the time course of blooming]
We have addressed these challenging questions using the American pawpaw (Asimina triloba), as a model system. Pawpaws are common American understory trees with burgundy colored, chamber-like flowers whose scent devolves from yeasty bread dough to sweaty athletic socks as the flowers age. My first PhD student, Kate Goodrich, identified several compounds common to fermentative microbes and hypothesized that flower-symbiotic microbes, in fact, may contribute to the scent of pawpaw flowers. More recently, Kyle Martin devoted his thesis to thoroughly testing the holobiont hypothesis.
Working with Roli Wilhelm and Dan Buckley, Kyle characterized flower part- and developmental stage-specific differences in microbiome composition, then used Koch's Postulates to test to what extent components of the floral microbiome contribute to the fermented function of pawpaw flowers. Topical sterilization reduced production of several key volatiles, and sterilized flowers were significantly less attractive to Glischrochilus sap beetles, the primary pollinator in our study population. Cultured microbes from pawpaw flowers emitted similar scent bouquets to those of control flowers. When culture pastes were added to sterilized flowers, they rescued beetle attraction to sterilized flowers, supporting the holobiont floral phenotype hypothesis.
[Left, timeline of pawpaw floral development, scent production and arthropod visitation]
[Left, timeline of pawpaw floral development, scent production and arthropod visitation]