Evolution of drought tolerance

Phylogenetic tree of 165 grasses. Size is bubble is proportional to physiological drought tolerance (big bubble = lower psi-crit).

We know a bit about the ancestor of Poaceae. All the main defining characters of grasses like the parallel venation, the monocotyledon, and the distinctive grass flowers, were present in the ancestral grass. What did the first grassland look like? What about it's ecology? Did grasses start in the shade and come out in the open? Were they from wet soils and evolved to inhabit the dry? 

We don't have a time machine, but we do have the ability to assemble the phylogentic relationships among grasses and infer origins. Steve Kembel helped out and took Erika Edwards phylogeny from her PNAS paper and arrayed physiological drought tolerance data from 165 species from our experiment that matched with her phylogeny.

The first thing that pops out is there is no phylogenetic signal to the data. Drought tolerance pops up throughout the phylogeny. If true--and our dataset is by no means definitive yet--then drought tolerance might be evolutionary labile. It might not take that many mutations to confer physiological drought tolerance.

But what about the ancestral trait? Was the mother of all grasses physiologically drought tolerant? That specific analysis has yet to be run, but likely not. Most of the modern grasses are not terribly drought tolerant and the most parsimonious explanation for that--as I understand it--is that it is more likely that the relatively small fraction of grasses that are super-drought tolerant hold the derived trait.

As they say, watch this space. We're going to try to prove ourselves wrong in the meantime.

Heat waves and drought: it's all in the timing

Distribution from 1984-2010 of (a) mean daily maximum temperatures averaged over 15-d intervals and (b) soil moisture at 25 cm taken approximately every 15 days. Also shown (c) is the sensitivity to grass aboveground net primary productivity (ANPP_G) to variation in drought and heat waves assessed every 15 d in 5-d increments. The critical climate period for drought (day of year 105-214) is shown in blue and for heat waves (day of year 190-214) is shown in red.

July in 2011 has been hot. And dry. Supposedly it's suppose to be like this more often in the future as future climates are likely to include more frequent droughts and heat waves. 

It's generally assumed that in most grasslands these events reduce grass production, yet their effects have been viewed somewhat monolithically. When it comes to forecasting the consequences of future climate variability, droughts and heat waves in early-, mid-, or late-summer are not viewed very differently. Absence of evidence is not necessarily evidence of absence though. 

The Konza LTER has built up datasets over the past 25 years that can really test this, though.

27 years of annual productivity

27 years of daily weather

27 years of daily stream discharge

27 years of biweekly soil moisture

17 years of biweekly productivity

11 years of remotely-sensed NDVI

I'll write about some of the datasets another time, but if one examines the annual productivity data and the climate data together with the critical climate period approach, it is clear that the timing of climate variability is just as important--if not more--than the magnitude.

First, grass productivity only responds to drought (or the converse precipitation) during part of the growing season (Apr 10-Aug 2). Drought in August doesn't reduce primary productivity. 

And heat waves? They only reduce productivity during a 25-d window. Jul 10 - Aug 2. Heat waves in August, no less June, just have no impact on productivity. 

We can use these data to come up with new relationships between productivity and climate variability.

A couple of lessons can be learned here, but the most striking is that droughts and heat waves in August just don't affect grass production. It's not that grasses aren't growing then. About 10% of the production happens then and in some years it can be as high as a third of the mean annual productivity. Yet, growth during that time is not tied to climate then.

It's hard to explain why this is so, but the practical consequences are clear. If droughts or heat waves are more likely to happen in August, it doesn't matter for the amount of grass we have. We've shown elsewhere it still impacts the bison, most likely because they cue in on grass quality than quantity. But ANPP is insensitive. If we  want to predict future productivity well, they we better know timing as well as magnitude.

**On a side note, the results are really the highest expression of what the LTER approach can accomplish. I think long-term datasets have fallen out of fashion in the ecological community. When was the last time Science or Nature published a paper that centered on a long time-series from an LTER site. Compared to experiments, models, and cross-site synthesis, long time series seems like a short leg of the table these days. No one has ever set up an experiment to test what natural variability has shown us about the timing of variability.

Grasses of the World IV--Taxonomic differences

Relationships between leaf width and physiological drought potential for six genera of grass.

No one know exactly what the ancestral grass looked like or the environments it inhabited. But one could imagine a bright, open wet environment with a narrow leaved bunch grass or weakly rhizomatous grass inhabiting it.  Some tens of millions of years later the BEP and PACMAD clades would have diverged and the major radiations of grasses still a long way off. 

But what were the forces that drove the radiations. Aridity is often cited as one. Fire another. Grazers still a third. But this might be somewhat of a skewed, biased perspective, since there has been little work to characterize the modern ecology of the whole of grasses.

When we look at the global traitscape of grasses, we saw clear patterns for leaf width and drought tolerance. One can imagine some selective force favoring wide-leaved grasses and drought narrow leaved grasses, until an ecological or physiological tradeoff was reached.

But what does the pattern of radiations for individual clades look like?

If I map the distribution of 6 genera in traitspace, clear unique patterns show up. The genus Panicum, for example, has species with wide and narrow leaves, but none that are very drought tolerant. In contrast, Festuca species all have leaves that are narrow, but span the full range of drought tolerance.

We still haven't mapped all this onto a phylogenetic tree. That's coming. But the value of screening programs like this are pretty clear for understanding the ecology and evolution of grasses. 

But why the separation among genera? Are individual genera constrained physiologically, or are they constrained evolutionarily by the presence of other species that lead to the apparent differentiations. 

Part of what we still need to do is understand the importance of traits such as leaf width and understand the benefits (and constraints) of narrow and wide leaves.

Traitscape of drought tolerance for Konza

One of the keys to understanding community assembly will be assembling traitscapes for communities and comparing them to global traitscapes. Earlier, I showed how we could assemble a nitrogen traitscape for Konza and compare that to the global distribution to show that the typical Konza species has higher foliar N concentrations and experiences higher N availability than the typical species at the global scale.

We're getting close to being able to do something similar for Konza, but for physiological drought tolerance. We're working to collect all the grass species of Konza and measure their psi-crit in order to compare them to the global distribution. We've only fully measured 28 of Konza's 86 species of grasses, but the patterns so far our interesting.

Part of the power of the traitscape is to understand inter- vs. intra-site importance of environmental variation. For drought, if we expect Konza to be more likely to experience frequent and severe drought than other grasslands of the world, you could expect to see the typical species be more drought tolerant than the global distribution. We can also look at the distribution of drought tolerance at a site and see how that compares to the global range. Means might be different, but if there is high spatial or temporal variability in water availability, a community could encompass a large part of the global range.

Expectations for Konza are a bit uncertain--it's a humid prairie (835 mm y-1 precip), but can experience severe droughts. Within site, there are dry habitats--south facing slopes with thin soils--and wet ones--seeps, riparian areas, and ditches.

The pattern?

So far the global mean psi-crit is -4.8 MPa. Konza? -4.5 MPa.

The global range is -1.4 to <-14 MPa. Konza? -1.8 to -13 MPa.

Here's the pattern of psicrit with leaf width (red = Konza species):

After 28 species, most of the global trait-space is covered. If anything, Konza might be underrepresented in fine-leaved, drought tolerant grasses. I haven't measured Agrostis hyemalis yet, but it's leaves are about 1mm across--we'll see how drought tolerant it is.

I think there's an amazing range of diversity in drought tolerance at a single site. Konza might be an exception, but the diversity in soil moisture availability at a site can be high.

One question that comes up is that if there can be such high diversity at a site, what are the differences in among sites? How important is drought tolerance in differentiating grasslands and contributing to gamma diversity?

Grasses of the world III--grasses can be incredibly drought tolerant

I've posted that I've been growing up 500 grass species from around the world to look at the geographic and phylogenetic distribution of physiological drought tolerance. Before we learned we were a bit constrained in quantifying the drought tolerance of grasses because we had grasses that could withstand pressures in excess of our previous pressure bomb, which maxed out at 10 MPa (~1450 psi). Jeff Hamel at PMS Instruments sent us one that goes to 14 MPa (~2000 psi). With that, we've rerun some grasses and measured some new ones, while we wait for some others to grow from seed again.

Still, the first results show that there are grasses that are incredibly drought tolerant.

We've now measured physiological drought tolerance (psi-crit) on 398 species. 13 of those were able to conduct water at pressures in excess of -14 MPa. That's more than 3% of the grasses we surveyed.

3% does not seem like a large number, but that number will only go up as we measure the most drought-tolerant species which are regrowing. 5% might not seem that high, but that'd be 500 species of grasses in the world if you extrapolate out. 

How drought tolerant could some of these species be? If you extrapolate out the lower bound of the width-psicrit relationship, we should have some that hit -17 MPa (~2500 psi).

Drought tolerance: grasses of the world II

After 200 species, there still is a boundary between width and drought tolerance, just with a missing corner.

I haven't seen too many reviews of drought tolerance/cavitation resistance of grasses, but it is generally thought that permanent wilting points for most grasses is about -3MPa. It isn't considered that too many plants can resist below -10 MPa. Why -10 MPa? Because the machines to measure water potential don't go below there.

In the past few weeks, I've continued to measure the drought tolerance of grasses from across the world.
As the species have accumulated, the same tradeoff boundary observed earlier appears to hold. Yet, over 10% of the species appear to be able to conduct water at pressures below -10 MPa. For reference, if you could graft any of these species on the top of the tallest redwood, they could still conduct water.

We still need to nail down the actual psi-crits for the species. The problem is that our pressure bomb stops at -10MPa (100 bar).



The good news is that Jeff Hamel at PMS has been kind enough to build one that goes to -14MPa, which should allow us to determine the drought tolerance of the most drought-tolerant grasses. We'll grow up these species again and let them dry down. Hopefully, Jeff won't have to build one that goes below -14 MPa.

Drought tolerance: grasses of the world

One of the 500 species that are part of the Poa500 project to examine drought tolerance in grasses of the world.

I'm not sure this one is going to work. I believe that if you measure something interesting and have strong contrasts, you should learn something interesting. I've had pretty crazy schemes work out in the past. Hopped on a plane and measured roots on three continents. Had people send me soil from across the US to look at nutrient limitation. Measured foliar 15N for a couple hundred species at Konza. Even looked at spectroscopic assays of 20,000 cow poop samples to infer continental scale patterns of forage quality.

Each time, we learned something interesting by having strong contrasts and measuring something interesting. But to start to understand global patterns of drought tolerance by growing 500 species of grass in the growth chamber in relatively tiny tubes? I'm just not sure this one is going to work. 

Granted, what we're doing right now is just a pilot project and would be easier with the NSF Dimensions of Biodiversity grant funded. But, questions about the evolution and geographic distribution of drought tolerance are just too important not too try. At the heart of it, we just don't understand the traits that are associated with drought tolerance--what does a drought-tolerant plant consistently look like. In what climates are they most likely to be found. Are some lineages more likely to have evolved drought tolerance than others?

To begin to answer the question, USDA sent me seeds for 500 grass species from their seedbanks and I've serially germinated them over the past 2 months. After about a month, we measure a couple of gas exchange and morphological metrics on the leaves and then stop watering. When they stop conducting water (shut their stomata), we measure their water potential, which we call psi-crit.

A little over 100 species have hit their psi-crit so far. Here's probably the most interesting graph so far--drought tolerance (psi-crit) vs. the maximum width of the largest leaf on the plant. 

It seems like you can have narrow leaves on plants that aren't drought tolerant--species like Enneapogon oblongus. You can also have narrow leaves on plants that are drought tolerant--species like Bouteloua repens. You can also have wide leaves on plants that are not drought tolerant--species like Dichanthelium scoparium. But you can't have wide leaves on plants that are drought tolerant. Doesn't exist.

Of course, it doesn't take more than one species to prove something not impossible.

We still have a few species left to measure, of course.

The model species set

By restricting our own freedom, we gain collective power. It's a tenet of larger society, but also scientific society. 

For some the restriction is in the form of Arabidopsis. Zea for others. Populus, Lotus, Medicago...the list of model organisms that are used to answer fundamental questions about the genetics of plants goes on.

But what about the evolution of plants? To a degree, we can compare the genomes of model organisms to hint at some of the broader evolutionary patterns. But evolutionary patterns are generally derived by comparison with multiple members of a single clade. If one wanted to understand the evolutionary patterns of grass, we couldn't just look at a single model organism. We would need to look at a model set of species.

What would a model species set for grasses look like? It would have to be large enough to cover the major clades (~10), but restricted enough that researchers could measure standardized metrics on every species. Probably about 100 species. For grasses, they should come from different continents, span multiple origins of C3 and C4, and cover a wide range of environmental tolerances. Seed should be readily accessible. Most likely seed sets would have to be collected by a central agency for distribution to willing researchers. A central database would be needed to store all the data for other researchers to use.

Once that happened, an individual researcher that was interested in the cold tolerance of grasses could grow up all 100 species, measure their cold tolerance, and then examine the evolutionary patterns of cold tolerance. The next researcher that wanted to examine stomatal density could do the same, and then would be able to compare it with cold tolerance. Root anatomy, mycorrhizal dependence, genome size, carbonic anhydrase activity, flowering phenology, drought tolerance...the database would build. Each time we would learn more about multivariate trait selection in ways that no one lab could do.

Why doesn't this exist? Hard to say. Part of it is probably some small group just deciding which 100 species to use. Would it be perfect and cover all the potential evolutionary questions? No, but there are researchers that are asking these questions anyways, so they might as well be using the same species. Plus, there always could be a second species set identified to fill the gaps in the first for a second round of measurement.

Why not just keep a database and let researchers work on whatever species they felt best allowed them to examine specific ecological and evolutionary contrasts? Never enough overlap. Brassicaceae has 3700 species and even the Arabidopsis genus has 9 species. But everyone works on thaliana even if other crucifers might be better to answer some questions.

Once the scientific community agrees to encourage the restriction of freedom of inquiry into plant evolution a little more, a large amount of collective power will be realized. How long should it take? A few informed individuals who are not afraid to make political sausage would need to be in the same room for about 2 days. How long will it take to get people in a room for 2 days? Hopefully within a year or two.