Feeling the heat

(Press-News.org) Brace yourself for a hot story about plant sex.

Harvard researchers have discovered that cycads—one of the oldest living lineages of seed plants—heat up their reproductive organs to attract beetle pollinators and the insects possess infrared sensors to detect these signals. First the male cycads warm their pollen cones to entice beetles and then the female plants similarly get hot and the insects follow—and thereby spread the genetic material enabling the plants to reproduce.

The new study [LINK WILL ACTIVATE WHEN EMBARGO LIFTS 2PM THURS 12/11 ], published Thursday in a cover story in Science, marks the first time that infrared radiation has been identified as a pollination signal—one far older than the splendorous colors that later become dominant among flowering plants.

“This is basically adding a new dimension of information that plants and animals are using to communicate that we didn't know about before” said lead author Wendy Valencia-Montoya, PhD ’25, a junior fellow in the Harvard Society of Fellows. “We knew of scent and we knew of color, but we didn't know that infrared could act as a pollination signal.”

In fact, heat may be one of the most ancient modes of communication between animals and plants and even predate the dinosaurs. “Long before petals and perfume,” said Valencia-Montoya, “plants and beetles found each other by feeling the warmth.”

The findings shed new light on the ancient alliance between plants and pollinators and culminates a scientific quest that stretched more than a dozen years since Valencia-Montoya began studying cycads as an undergraduate in Colombia.

It has long been known that many plant species warm their pollination cones or flowers by cranking up their metabolism. “But everyone assumed that the heat was mostly just to help volatilizing scents,” said Valencia-Montoya, who found it puzzling that plants would invest so much energy in heat production.

After coming to Harvard for her PhD, she planned to continue research on cycads in South America but was forced to adjust her plans during the pandemic. Instead, she conducted most of her research at Montgomery Botanical Center in Florida. Her work was supervised by Professor Nicholas Bellono of Molecular and Cellular Biology and Naomi Pierce, Sidney A. and John H. Hessel Professor of Biology in the Department of Organismic and Evolutionary Biology (both coauthors on the new paper).

As the oldest known seed plants pollinated by animals, cycads are sometimes called “living fossils” and have long aroused fascination among biologists, The plants have stout trunks and crowns of featherlike leaves and resemble palms and ferns, but are not closely related to either.

Cycads appeared around 275 million years ago and reached their peak diversity around 150 million years ago during the Jurassic period. They were largely displaced by the rise of flowering plants, which became the dominant group in the last 70 million years.

Today about 300 cycad species remain, most of them listed as endangered.

Cycads so called “dioecious” plants because they have male and female individuals distinguished by their reproductive cones. Male cones produce pollen and female cones bear ovules that, if fertilized, develop into seeds.

In the new study, Valencia-Montoya and her colleagues focused on Zamia furfuracea, a four foot-tall cycad native to Mexico commonly called “cardboard palm.” Like every cycad, it has an exclusive symbiotic relationship with its own pollinating beetle species—Rhopalotria furfuracea, a small, long-snouted brown weevil.

In a “push-pull pollination” relationship, cycads use a combination of signals including heat, odor, and humidity to attract beetles to feed on pollen in the male cones. At a certain point, these signals become so overwhelming that the beetles are driven out of the male plants towards the female ovulate cones. “It's sort of like a guy puts on cologne to go out on a date,” explained Pierce, “a little bit is a nice thing, but too much is repulsive." By migrating between plants, the beetles transmit male pollen and fertilize the seeds in the female plants.

But how did heat factor in this ancient relationship? Valencia-Montoya and her colleagues took thermal images and found that cycads heat production focused on the cones. The parts bearing the reproductive organs, the sporophylls, contained high concentrations of energy-producing mitochondria. Zamia furfuracea could heat its cones 46 degrees Fahrenheit above the ambient air temperature, but other cycads could get even hotter.

The researchers examined 17 cycad species and discovered that all followed a circadian pattern at the end of the day: first male cones heated and then cooled down and about three hours later, females cones began to warm.

Next Valencia-Montoya and her colleagues tracked movements of the beetle pollinators by marking them with ultraviolet fluorescent dyes and watching at night as they moved between plants in an open field. The beetles were attracted to the warmest parts of the cones—first the males, then the females.

“This was one of the early compelling pieces of evidence that this is probably related to pollination,” said Bellono. “Male and female plants were actually heating in a circadian-controlled manner—and we could see it locks with the beetle movement.”

Next the researchers investigated the pollinators: How did beetles sense the heat?

In insects, the main sensory organs are the sensilla, the hairlike structures on the antenna. Using techniques such as electron microscopy, electrophysiology and transcripts of genes expressed in the cells, the researchers discovered that beetle antenna tips have specialized thermosensitive organs packed with heat-sensing neurons. One key molecular sensor was a protein TRPA1, which is also employed by snakes and mosquitoes to sense warm-blooded prey.

These organs were calibrated to the specific heating temperature of the cycad. Researchers examined another beetle species and discovered it too had sensation range fine-tuned to the specific heating temperature of its own cycad host.

The researchers believe that heat-generation evolved near the origins of the cycads some 275 million years ago and might be the oldest known pollination signal.

Until now, “push-pull” pollination was believed to be mainly driven by scent. The new study suggests that this relationship probably also was hot from the start.

At close range, scent becomes less effective and infrared radiation can guide pollinators to their target.

Heat-producing plants tend to be from ancient lineages (cycads account for about half of them). In the grand scheme of plant evolution, the importance heat waned and color rose. Eventually, the drab-colored cycads were outcompeted by the explosive radiation of colorful flowering plants—and their pollinators such as bees and butterflies evolved keener visual senses. (Most beetles have only dichromatic vision and poor color perception while bees have trichromatic vision and butterflies have tetrachromatic vision.)

The fact that the infrared signal had remained unrecognized for so long probably reflects our own sensory bias.

“All the sensory cues that have been recognized very fast are the ones that we can perceive," said Valencia-Montoya. "But the ones that are hidden may be as important.”

 

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