THE EVOLUTION OF LEAVES

This update relates to a "theory" for the origin of leaves by Osborne et al. 2004, a long version of a 2001 paper in Nature. Osborne et al. worry about the fact that it took about 50 m.y. for vascular plants to evolve leaves. They suggest that the delay was caused by the inevitability that leaves, if they evolved earlier, would have fried.

Here is Carl Zimmer's blog on the paper, which is basically an elegant re-statement of their thesis.

Problems with the ideas of Osborne et al.
As explained on p. 97, stomata on plant leaves take in carbon dioxide from the air to supply the photosynthesis that goes on inside the leaf spaces. Because they are open, stomata can lose water from the plant, in the form of water vapor that diffuses out as carbon dioxide diffuses in. The water vapor evaporates from the plant tissues inside the leaf. Living plants are often water-stressed, so they close the stomata when photosynthesis is not operating (at night, for example). But that is only a general observation, not a requirement.

Carbon dioxide levels were globally high in mid-Paleozoic times, say Osborne et al., so any proto-leaves would have needed comparatively few stomata to take in all the carbon dioxide they would have needed. As a result, proto-leaves would not have been evaporating much water. Evaporation cools a surface if fluid is evaporating from it (evaporation of sweat cools your skin if you sit in a breeze). A slow rate of evaporation would not cool a leaf very much. Osborne et al. seize on this biophysical fact to speculate that early vascular plants would have fried if they had evolved leaves: the added solar radiation shining on the leaf, combined with the lack of evaporative cooling, would have resulted in "lethal overheating," in their phrase.

Then 50 million years later, say Osborne et al., carbon dioxide levels and global temperatures dropped in the Late Devonian, making it finally possible for leaves to evolve without frying themselves. Leaves would now need many stomata to take in the carbon dioxide they needed, so they would have generated much more evaporative cooling; and they did. QED.

Obviously, I've simplified, but not much.

This construct depends absolutely on the assumption that leaves must close their stomata if and when they have taken in enough carbon dioxide for their photosynthesis, so they can no longer operate evapotranspiration for cooling. Any such closure would have had to relate to some reason connected with oversupply or overconcentration of carbon dioxide inside the leaf. This assumption is not discussed in Osborne et al. or in their previous paper in Nature.

What downside might there be to keeping the stomata open to promote evapotranspirative cooling? The only two possible results would be greater water loss, and greater intake of carbon dioxide.

  1. Water loss might be a problem for many plants living today, which often live in dry soils and dry air. But it was probably not important for early swamp-dwelling vascular plants.
  2. An oversupply of carbon dioxide might give mild acidification in the leaf spaces? However, carbon dioxide gets into the leaf spaces by diffusion, so, other things being equal, would never exceed atmospheric concentration. Even in the "high" carbon dioxide atmosphere of the Middle Devonian, these are not dangerous levels, even if the leaf cells continued to metabolize, thus producing carbon dioxide themselves. High carbon dioxide levels are apparently well tolerated by many plants today, so it is not much of a problem.

Therefore, on my simplistic assessment, the theory is based on assumptions so dubious that it cannot stand. I would have thought that the final invention of leaves and tree structure in the Late Devonian could have RESULTED in the carbon dioxide drop, rather than the reverse! Obviously it still took a long time for leaves to evolve, but I don't think we have a good answer yet. I'd be a poor botanist if all I did here was to criticize the idea of Osborne et al. without offering a better one: however, I am a poor botanist. Even so, I think I see a way through the problem, and I post it here for your enjoyment. I haven't done the necessary background work to polish it up, but I'll go with it until I do, or until you or other colleagues comment. Two colleagues who are plant physiologists have indicated that the remarks above are reasonable, but they are not to be held responsible for the rest of this essay, which asks:

Why Did Leaves Evolve?
Leaves do more than photosynthesize. Essentially, they are extravagant expansions of the plant epidermis, increasing its surface area many times. Furthermore, they are typically studded with stomata, thus multiplying the gateways by which the leaves exchange gases with the atmosphere. The gases of most interest are carbon dioxide, oxygen, and water vapor, and. of course, all three are ingredients in the chemical reactions of photosynthesis. It's hardly surprising that Osborne et al. concentrated largely on photosynthesis as they worried about the origin of leaves.

Stomata encourage evapotranspiration, where water vapor evaporates from the plant. Osborne et al. concentrated on the evaporative cooling that is an automatic result of transpiration, and their model focussed on the inability, as they see it, for the stomata to cool leaves in the high carbon dioxide atmosphere of the Middle Devonian.

But there is another aspect of evapotranspiration, one that may be much more significant for the origin of leaves. Evaporation (transpiration) from stomata high on the plant sets up a pressure gradient, a pump, that produces upward flow in the xylem of the plant. Fluid in the xylem flows upward from the roots to the leaves, carrying essential nutrients with it. Without such flow there can be no growth of the tissues high in the plant. The pressure of the pump is the same whether there are 2 stomata or 20,000, but the flow that is generated multiplies with the number of stomata. Your car battery produces 12 volts, but you need a bigger battery (more amps) to start a farm tractor than you do to start a Ford Escort.

Suppose an early plant has stomata in its stem, but has no leaves. The stomata can evaporate water vapor and set up a pressure gradient, but the flow of the nutrients is going to be low, so growth rates must be low.

Now suppose the plant evolves protoleaves. The increased stomata increase the nutrient budget delivered to the top of the plant, so it can grow higher and faster, increasing the stomata as more protoleaves are added, and so on. At the same time, photosynthesis increases, so that there is an increased downward flow of carbohydrates to the rest of the plant. This does not produce a plant that is vastly different in basic structure from its ancestor (yet), but such a plant might have a distinct advantage in an environment where faster growth yields higher reproductive success.

My most important point is that the addition of leaves by itself will not accomplish much. Leaves in higher plants are part of a system. The origin of leaves would have evolved side by side with increased capacity of xylem and phloem, to accommodate the increased reciprocal flow of nutrient-bearing fluids up and down the plant. There would be no point in evolving leaves if the roots were not gathering and transmitting nutrients from the soil efficiently. And the whole structure of the stem would have been expanded and strengthened to accommodate the transport system, and to bear the weight of the added leaves and their support branches.

So what we see as the "evolution of leaves" is just a part of the evolution of an integrated yet differentiated higher plant, with increasingly different functions operating in increasingly different anatomical regions. [It's not my fault that calculus has pirated these words to describe manipulations of abstract functions: I'm talking about real aspects of real plants here.]

The next level of question is evolutionary and ecological, and it goes back to the original conundrum which Osborne et al. failed to explain: why was it 50 million years between the evolution of the first vascular plants and the elaboration of those plants that Osborne et al. see mainly as "the evolution of leaves"?

I can offer some suggestions based on my story as outlined above. The first vascular plants were small (low to the ground) and apparently lived in tropical swamps. In such environments, evapotranspiration doesn't work very well (humans sweat profusely if they exercise in hot humid environments, but the sweat doesn't evaporate easily and the human quickly overheats). In plants, slow evapotranspiration means low pressure gradients in the vascular system, low nutrient flow, and overall a small energy budget. Plants cannot grow high, and sophisticated transport systems are not needed, so don't evolve: and that includes size, strength, and complexity of phloem and xylem; size, strength and complexity of roots; and leaves.

If I were to formulate a decent research project to analyse this further, I'd look as carefully at the root system as Osborne et al. have looked at evapotranspiration and cooling. Here's why.

If leaves didn't evolve, [and Osborne et al. don't have the right answer], it's because some other parameter in early plants didn't (yet) make leaves worthwhile. Why would increased photosynthesis not be a good thing? My suggestion is that extra nutrition from photosynthesis doesn't do any good if the growth of the plant is handicapped by lack of soil nutrients. In other words, the root system wasn't working up to modern standards.

As long as early plants were low to the ground, and small, their nutrient budget would have been small, and neither the system for getting nutrients out of the soil nor the system for pumping it round the plant would have been sophisticated. In fact, the ability to form leaves, and the trunk, branches, and twigs that would supported them, could not have been financed. It takes a lot of energy to build plant structures before leaves are budded, even in today's seedlings.

Roots today operate an ion pump to take nutrients from the soil, put them into the root system, and keep them there. This process generates a pressure, called "root pressure", that can move the nutrients round the plant. In addition, many plants today have accessory colonies of fungi called "mycorrhizae" associated with the roots. Mycorrhizae concentrate nutrients from the soil and essentially drag them close to the roots, making the whole process cheaper for the plant: but the mycorrhizae in turn are "fed" by the plant. This is another "high-budget" operation, which costs more but gives a higher return.

I suggest, then, that the evolution of larger plants was initially fuelled by nutrient supply rather than photosynthesis. Once the nutrient supply was large enough and efficient enough, the plant could "afford" the investment in larger size (mainly height) that involved building stem (trunk), branches, and leaves to increase photosynthesis (interest income on the investment).

I would expect that Devonian root systems would show evolution toward an advanced state along with advances in all the other systems I have listed. There is evidence of fungus associated with plants as early as the Middle Devonian Rhynie Chert: it's not clear (to me) that they were performing as mycorrhizae yet, and I am not sure how we could tell that. The fungal association is a complex game between plant and fungus, and it may have begun as a parasitic association before the current mutualistic stand-off evolved. Gary Vermeij suggested to me that it might have been the evolution of the mycorrhizal symbiosis that triggered major land plant evolution late in the Devonian.

Why and when and how should this major change in Devonian plants have occurred? The answer has to be ecological. If plants were to colonize habitats out of the swamp, out on to marginally or seasonally drier areas, with better-drained soils, evapotranspiration would have been a more powerful agent able to drive fluids to greater heights. Plants could have grown higher, and would have evolved bigger pumps (leaves), better hydraulics for circulation (larger and more organized phloem and xylem), and better supplies of nutrients from below (from the roots) and of fuels from above (photosynthates from leaves). It's also possible that mycorrhizae dictate that their plants grow in soils that are not swampy (waterlogged).

As I have discussed, all this requires a larger, longer investment in plant growth. Plants would have become larger, more sophisticated, and longer-lived. There would have been a differentiation between adaptations of a seedling and adaptations of an adult (a much more pronounced life-cycle sequence). I expect there would have been evolutionary pressure to evolve a larger seed, to give a young plant a quick boost off the ground as it germinated. But my brain is tired, so I'll stop here.

I am arguing for an evolution of a whole-plant system rather than for an evolution of a piece of a plant (a leaf). Trying to think about the "origin of leaves" as an isolated problem is too simple, given that we are talking about a complex organism. It's like trying to talk about "the origin of the erect limbs of vertebrates" as a question all on its own, when it's really a question about stance, locomotion, energy, respiration, circulation, physiology, behavior, ecology, and evolution all at once. Changes in posture, locomotion, and respiration associated with changes in body temperature happened in synapsids leading to warm-blooded mammals, and in diapsids leading to warm-blooded dinosaurs and birds. [If you're a student who's just got this far in the book, you'll soon find out about this question: and it's a great story!]

References:
Beerling, D. J. et al. 2001 Nature 410: 352-354.
Osborne, C. P., et al. 2004. Biophysical constraints on the origin of leaves inferred from the fossil record. PNAS 101: 10360-10362. Available on the Web.

First drafted by RC, October 5, 2004.

Updated December 27, 2004.

Links checked October 2, 2005.

Thanks to Terry Murphy, John Raven, and Gary Vermeij; but they fed me facts and principles, and any misuse of their help is my fault, not theirs.

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