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How Hot Does Your Pepper Grow? Depends On The Weather

One of my passions as an evolutionary biologist is understanding the balance between different forms of particular traits expressed within a population, especially either-or traits such as eye colour. I‘ve written about evolutionary trade-offs in birds, but birds aren’t the only living things where we can see this phenomenon. I was delighted to run across an elegant hot-off-the-presses study of chili peppers by a group from my alma mater, the University of Washington.

Even though chili fruits are popular amongst humans for being hot, they didn’t evolve this character to keep foodies and so-called “chili-heads” happy. Previous research indicates that chilies, Capsicum species, evolved their characteristic “heat” or pungency as a chemical defence to protect their fruits from fungal infections (doi:10.1073/pnas.0802691105) and from being eaten by herbivores. Chili pungency is created by capsaicinoids (kap SAY sin oids), a group of molecules that are produced by the plant and sequestered in its fruits. Capsaicinoids trigger that familiar burning sensation by interacting with a receptor located in pain- and heat-sensing neurones in mammals (including humans).

In contrast, birds receptor protein is different to mammals’, which is why their pain- and heat-sensing neurones remain undisturbed by capsaicinoids, so they can eat even the hottest chili fruits with impunity. Additionally, because birds lack teeth, they don’t damage chili seeds, which pass unharmed through their digestive tracts. For these reasons, wild chili fruits are bright red, a colour that attracts birds, so the plants effectively employ birds to disperse their seeds far and wide.

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Since pungency is such a favourable trait, it might surprise you to learn that wild chilies are not universally blazing hot. This certainly surprised then-graduate student David Haak as he and his colleagues munched their way through the wild chilies in southeastern Bolivia. Dr Haak’s colleagues, evolutionary ecologist Joshua Tewksbury, his thesis co-advisor at the University of Washington in Seattle, and tropical ecologist Douglas Levey, who was the postdoctoral supervisor to Dr Tewksbury at the University of Florida in Gainesville, also helped with these studies of the wild chilies, C. chacoense, in Bolivia.

“We would travel through rural Bolivia, eating peppers that ranged from milder than a Jalapeño to as hot as a Habañero”, writes evolutionary ecologist Dr Haak in email. Dr Haak, who studies local adaptation and ecological speciation, is currently a postdoctoral fellow at Indiana University in Bloomington.

Although the team confirmed that wild chilies vary considerably in the proportion of pungent plants in each population, they weren’t exactly sure why.

“We knew that chilies were hotter in wetter areas but we were not aware of the relationship between dryness and non-pungency”, explained Dr Haak in email.

Dr Haak was intrigued: What was the source of this variation of pungency in wild chili fruits? Were the plants making an evolutionary trade-off? If so, what was the basis for this trade-off? Dr Haak proposed that water availability might be the critical factor.

“Doug and Josh thought [this idea] was a long shot — and thus a good first project for a grad student.”

Undeterred by his colleagues’ confidence, Dr Haak sampled 21 chili populations in southeastern Bolivia located along a 300km north-south transect. These populations occur along a natural moisture gradient, with the southernmost locations being wettest. Dr Haak confirmed this from local rainfall data.

“Fortunately for me, there are several Mennonite colonies near our field sites and they kept daily rainfall records for 20 years”, writes Dr Haak.

He mapped chili pungency (pie charts) and rainfall data (coloured areas) against latitude and longitude and discovered a striking relationship (Figure 1a):

Five years of census data revealed that pungent chilies composed just 15–20 percent of the population in the drier northeast, whereas the wettest southeastern populations were comprised entirely of pungent plants. The small pie charts superimposed on this figure show the relative proportions of pungent plants amongst the new seedlings in each population sampled (white: non-pungent; black: pungent; figure 1aembiggen).

Dr Haak then used these data to build a mathematical model to describe the change in pungency within chili populations in relation to rainfall, independent of location, and found a linear relationship (Figure 1b):

To test this model, Dr Haak chose three chili populations with different proportions of pungent plants for more intensive study (triangles: black, 29% pungent; grey, 45% pungent; white, 88% pungent; figure 1bembiggen). Dr Haak and his team collected fruits from pungent and non-pungent plants in these three populations, and the seeds were grown in the university glasshouse.

The team selected 11 maternal lineages from the pungent and non-pungent plants for a total of 66 lineages comprised of 330 individual plants. These maternal plants were grown in the university glasshouse under the care of the study’s co-author, Leslie McGinnis, who was an undergraduate at the time. Seeds from self-fertilised (“selfed”) fruits were selected to form the population of study plants.

Initially, the study plants were all grown under well-watered conditions to ensure they all attained comparable sizes. When they began flowering, half of the plants in each lineage were assigned to one of two treatment groups; one group continued to be well-watered (WW) whilst the other was water-stressed (WS). Rainfall data from the dry field site were used to determine both the amount of water that WS plants received and the timing of those water restrictions. After the study plants bore fruit, the team collected them and counted the total seed output for pungent and non-pungent plants under WW and WS conditions (Figure 2):

They found that WW plants produced equal numbers of seeds, but under WS conditions, pungent plants produced 50 percent fewer seeds than did non-pungent plants (figure 2; embiggen). So there is a clear water-dependent trade-off between seed production and pungency in chilies, but why?

Plants lose water through microscopic pores in their leaves and stems, known as stomata (singular; stoma). During the day, plants release oxygen to the environment in exchange for carbon dioxide through their stomata, but this vital gas exchange comes at a price: water loss. Knowing that the density of stomata on a plant’s leaves directly affect water loss, the team compared stomata density from 30 age- and height-matched pungent and non-pungent chili plants (figure 3):

They found that pungent plants have a 40 percent greater stomata density on their leaves than do non-pungent plants (figure 3; embiggen). Even after cross-breeding pungent with non-pungent plants and then identifying whether the fruits were pungent, the team found that the pungent crossbred chilis still had a greater stomata density than did the non-pungent crossbreds.

Thus, different populations of chili plants are making fitness trade-offs between pungency and non-pungency based on local water availability: wetter environments supported a higher percentage of pungent plants, whereas drier areas had significantly fewer pungent plants. Even though chili fruits in drier environments were less likely to be destroyed by fungus, Dr Haak noted that 90 to 95 percent of the fruits had some level of fungal infection, but pungent plants were better able to defend themselves.

“It surprised us to find that the tradeoff to produce capsaicin in pungent plants would involve this major physiological process of water-use efficiency,” remarked Dr Haak.

Of course, this study also has important implications for devoted chili-heads and gardeners: be sure to provide adequate water to your habañeros.

Sources:

Haak, D., McGinnis, L., Levey, D., & Tewksbury, J. (2011). Why are not all chilies hot? A trade-off limits pungency. Proceedings of the Royal Society B: Biological Sciences | doi:10.1098/rspb.2011.2091

Tewksbury, J., Reagan, K., Machnicki, N., Carlo, T., Haak, D., Penaloza, A., & Levey, D. (2008). Evolutionary ecology of pungency in wild chilies.Proceedings of the National Academy of Sciences105 (33), 11808–11811 | doi:10.1073/pnas.0802691105


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