Evolution in a terrarium?

Our understanding of ecology and evolution has historically been highly stratified; with conceptual divisions and blinders between humans and the environment, between disciplines, and between substantive foci.

As a highly anthropocentric species, for a long period of time people thought that the rules of nature somehow didn’t apply to humans.  Arguably, even today, many who study human evolution do so in the absence of thinking about how evolution occurs in all of the other organisms on our planet.  To be fair, it is difficult to really delve into a subject without focusing on it – but I also think that a narrow approach can be dangerous too.  Furthermore, it’s probably easier to see evolution occurring in your favorite organism if that organism doesn’t have generation times that are as long as yours…

And this “us versus the rest of the world” type of thinking has extended both ways.  Not only do we evolve, but we are constantly modifying our environment.  We’ve probably been doing that for a very long time.  Given that most other organisms modify their environments – beavers build dams, ruminants alter landscapes by selectively grazing in certain areas – I would say that it’s silly to think that we haven’t been altering our landscapes for a long period of evolutionary time.

For a period of time in U.S. history, when manifest destiny and western expansion were the battle cry of the day, it wasn’t uncommon for people to arrive in environments, new to them, and to think of those places as pristine, untouched landscapes.  This is what much of our modern environmental movement grew out of.  We thought of these Western landscapes as things that hadn’t yet been marred by human hands, and we needed to keep them pristine for the next generation.  This was and is a flawed view of the relationship between humans and environment.

Long before Euro-Americans showed up in the American West there were native peoples living in these wide open spaces.  There were just a lot less of them when the new Americans showed up because new pathogens had already moved across the landscape, at a speed that would have been impossible for the new Americans to match, and completely decimated much of the population.  These beautifully manicured landscapes weren’t untouched.  They had been manipulated, lived in, and exploited for thousands of years prior to European arrival here.

The arrow goes the other way too.  We are modified by our environment.  Returning to my favorite subject (pathogens), the story of the sickle cell trait and malaria is a textbook example of how the environment, this time in the form of parasites spread through mosquitoes, has actually left an imprint on the human genome [1].  And considering that much of the evidence about the evolutionary history of falciparum malaria suggests a leap into humans around 10k years ago, humans may have started the ball rolling per se with the onset of agriculture.  The real story, however, is probably much more complex than the one(s) that anthropologists usually tell.

Humans began changing their environment to such an extent that it could have led to a population increase in a specific type (or types) of mosquito.  These mosquitoes were already in the environment, and would have already been capable of spreading a parasite that had also already been in the environment.  That parasite has recently been shown to occur in high prevalences in wild gorillas, meaning that agriculture wasn’t necessary for it to exist in human populations, but several lines of evidence suggest that agriculture could have been sufficient for it to be a major factor in human populations [2].  Furthermore, malaria parasites have coevolved with their hosts, with a multitude of adaptations that allow them to survive our (and other organism’s) immune responses [3]. 

Humans made a change to their landscape: agriculture.  That change may have reduced the risks associated with starvation, but also may have increased the population sizes of some pest species: mosquitoes.  And it wasn’t just any type of mosquito that would have been influenced, but a type or types which are capable of effectively spreading a parasite: falciparum malaria.  And that parasite has developed the ability to sexually reproduce in certain types of mosquitoes and to maintain population sizes within human hosts that don’t immediately kill everyone who is infected, therefore allowing the life cycle to continue. 

These coevolutionary relationships aren’t even close to being limited to the malaria story.  For example, a non-trivial portion of the human genome is made up of endogenous RNA viruses.  We’ve been shaping our environment, and it has been shaping us, for a very long time. 

This story isn’t just about pathogens though, because through domestication humans have transformed plants and animals too.  The list of such “domesticated” organisms is, like the list of pathogens with coevolutionary relationships with humans, too long to give proper space to here.  But think about the special relationships between humans, cats and dogs (they’ve arguably domesticated us).  Or between humans and yeast (see a nice blog post here), or with maize or potatoes, or cows and sheep.  The not so funny thing is, that while we know about all of these modifications that humans have made to the environment, and that the environment has made to humans, they almost always get studied in a highly stratified way.  As if each of these components occur by themselves, in a terrarium, not interacting with everything else. 

Plants get studied in botany departments or in schools of agriculture.  Insects are either studied by agricultural scientists (worried about what they’ll do to plants) or biomedical scientists (worried about what they’ll do to people).  Biomedical scientists who focus on the actual pathogens, in my view, tend to ignore the human component.  (Of course, a lot of interventions are based on killing something in the epidemiological cycle, and most people don’t want to take out the human host for the sake of the other components of the epidemiological cycle).  And finally, people who study human evolution are just as bad (or worse) than everyone else on this list; mostly ignoring the major evolutionary pressures (disease and nutrition) that have undoubtedly shaped who we are so that we can instead focus on topics that are sexy (to humans, that is).  Even though we know that humans do not live in terrariums.  Or most of us anyway.    

References:

1. Kwiatkowski DP: How malaria has affected the human genome and what human genetics can teach us about malaria. American Journal of Human Genetics2 2005, 77:171–190.

2. Liu W, Li Y, Learn GH, Rudicell RS, Robertson JD, Keele BF, Ndjango JBN, Sanz CM, Morgan DB, Locatelli S: Origin of the human malaria parasite Plasmodium falciparum in gorillas. Nature 2010, 467:420–425.

3. Evans AG, Wellems TE: Coevolutionary genetics of Plasmodium malaria parasites and their human hosts. Integrative and comparative biology 2002, 42:401–7. 

  

The rain in Spain falls mainly on the grain

We have several times in this blog pointed out the problem of too much hubris in science, the attitude that we already know everything important and therefore can be very sure of what we say. But maybe, like Eliza Doolittle in My Fair Lady, we scientists could use a bit of polishing before we speak so confidently, if we think we deserve to be taken seriously. Maybe this is an example (at any rate, it's interesting):

The Oct 21 episode of the BBC World Service radio program, Discovery, included a discussion of 'biopreciptation' (we'd link you to the podcast, but it has already been taken down; here's a link to an older version of the story on BBC Radio 4). The term 'bioprecipitation' was coined some 25 years ago by Dr David Sands at Montana State University, though it pretty much fell on deaf ears. With increasing evidence now, however, the idea that the biosphere may have a significant impact on climate is gaining followers.

Most rain and all snow falls as ice, but the water in clouds doesn't form frozen crystals at 32 degrees F, but rather some degrees colder, and almost always around ice-nucleating particles. These particles can include dust and pollutants, which have been the text-book explanation. But Dr Sands' and colleagues found, as reported in a Science paper last year (Ubiquity of Biological Ice Nucleators in Snowfall, Chirstner et al., Science 29 February 2008: Vol. 319. no. 5867, p. 1214), and recently on BBC radio, that some bacteria serve the same function, but they do so at warmer temperatures.

Christner et al. have examined snow and rain for the presence of nucleators. As reported in the Science paper, they found that 70 to 100% of the nucleators in snow that were active at higher temperatures were biological, and a majority of those were live bacteria. It turns out that most of these bacteria are plant pathogens, specifically Pseudomonas syringae. They infect, but don't necessarily kill plants, spending much of their time there, but they can be swept up into the atmosphere when conditions are favorable, where they drift with the winds aloft, later to form the core of rain drops or snowflakes, and then fall back down to Earth. Those that land on plants reproduce there, and then can be blown back up into the atmosphere, where they can become part of the precipitation cycle all over again.

So, these plant pathogens may contribute to rainy -- or dry -- conditions anywhere in the world, and there may be feedback loops. If an area is suffering from drought, vegetation may be sparse, and thus populations of these rain-inducing bacteria may be sparse, thus leading to less rain, less vegetation, and so on. It's possible that this kind of feedback is in part responsible for the droughts in Africa and Australia, according to Sands and colleagues. That means they can have continental, and hence perhaps in turn even global climate effects.

Christner et al. conclude their paper by saying:

Unearthing a role for biological [ice-nucleation] in the precipitation cycle has implications for deciphering feedbacks between the biosphere and climate, improving climate forecast models, and understanding atmospheric dissemination strategies of plant pathogens and other microorganisms.

This is a beautiful example of the interconnection of the biota on Earth in unexpected ways. But there's a further twist to the story. The ice-nucleating property of this bacterium is known; it's a protein on the cell-surface of the P. syringae bacterium. Intact bacteria, then, at the right temperature and given wet conditions, can nucleate ice formation directly on the surface of plants, causing potentially costly frost damage to crops. A form of the bacterium without the ice-nucleating surface protein, called 'ice-minus', occurs in the wild, but a lot more of them have been genetically engineered and introduced into fields where it's hoped that will have a man-made selective advantage and out-compete their ice-nucleating cousins--to do less crop damage.

Nice, neat story and a triumph for science and (we hate to admit it) big agribusiness, too. Right? Not necessarily!

Given the role of P. syringae in precipitation cycles worldwide, in ways not yet fully understood or even characterized, the possibility of disturbing it is rather alarming. If we seed the atmosphere with ice-minus bugs, and they out-compete the currently-prevalent strain, then there will be less crop damage but there will also be less cloud and rain formation. Cloud and rain formation affects climate, climate affects areas of drought and surfeit of rain, which can affect both climate on a large scale, and of course agricultural productivity. And if the patterns are altered the effect could, like the famous Lorenz butterfly effect of chaos theory, proliferate on a much larger scale.

How large? Enough to affect global climate or climate cycles? Could crop patterns already have had some effects on this interacting system, that we never suspected? Could this go back into history? Could global warming or other recent climate changes be due not to greenhouse gases alone but to agricultural paterns or technology in some significant way? These effects could, of course, turn out to be trivial, "a lot o' nowt wi' no clout" as Eliza Doolittle might say. It could even turn out that 'ice-minus' bacteria really do have a good effect without the bad. On the other hand....

The fact that bacteria are frequently the condensation nuclei around which ice crystals form and hence that are the source of cloud and precipitation illustrates the concept of 'dark matter' that first arose in physics and refers to things not suspected by science until in some way (usually by chance) they are discovered. Before that, we have our theories, that are shoes into which science tries to force the feet of data that we already know about, sometimes causing serious bunions. The lessons of the history of science are a repeated warning to us. We can't develop theories resting on evidence we don't know about, of course, and not everything we discover turns out to be important. But we can't be too sure of ourselves.

Like Eliza Doolittle, we can't win a prized companion if we can't speak the right language. Her pompous tutor Henry Higgins was cock-sure of what that right language was, but the outcome was ambiguous--as it often is in science, where the right language may always be changing, and we need to look constantly to Nature to learn what that is.