A wrench in the domestication of corn story

Holly and I are working on a book together, and it's fun.  It was her idea originally, and I just had the good fortune to be invited on.  So, imagine a book that includes discussion of things like sperm-ejecting hens, Koko the talking gorilla choosing how to expand her family, what the origins of agriculture have to teach us about sex, what sex has to teach us about the origins of agriculture, and so much more, and you'll perhaps be able to imagine why this is so much fun. 



This month I've been reading and writing a lot about the agricultural transition.  As most things, the more you learn about something the more you realize how little is actually known.  I thought I knew the history of the domestication of corn, say, but that was before I actually read anything about it.  

The Neolithic
For at least the last two million years of the evolution of the genus Homo, and for maybe even longer than that, reaching back into Australopithecus times, our ancestors foraged for food, collecting seeds, roots, fruits, eggs, and scavenging or hunting for meat and fish. This came to an end in much of the world some 10-12,000 years ago.

Since intention isn't preserved in the archaeological record, the reason for this will probably never be known, but possible explanations include population pressure; perhaps that foraging could no longer feed growing populations, or climate change; the end of the last glacial age, and the warming of the climate, which among other things may have brought changes in the availability of familiar wild foods.  

Why it happened at generally the same time around the world is a curious thing; first in the Fertile Crescent of the Near East, then in Mesoamerica, followed by Southeast Asia, although there is evidence that plants were being domesticated in Ecuador at about the same time as they were in the Fertile Crescent.  The fact that the transition to agriculture happened pretty much simultaneously everywhere suggests that global climate change was in fact that driver, but that's hard to demonstrate.

In any case, as far as is known today, plant domestication happened in 24 different regions, and in 13 of those regions grain crops were the primary focus. 

Centers of plant domestication; The nature of selection during plant domestication

Michael D. Purugganan & Dorian Q. Fuller, Nature 457, 843-848(12 February 2009)

Eight plants were domesticated in the Fertile Crescent; einkorn and eimmer wheat; barley; lentils; peas; chickpeas and bitter vetch, and flax. Rice was domesticated in Asia, potatoes and beans in South America, maize, and bottle gourd and squash in Mesoamerica, with many more as the agricultural transition progressed.     

Dogs were probably the first domesticated animal, about 35,000 years ago, from wolves, followed by cats near the time of the agricultural transition, but it's possible that both these animals were attracted to people and domesticated themselves. Cats may have been attracted to settlements because rodents would have lived in and around stored grain. 

Goats were probably the first animals domesticated for food, in the Fertile Crescent, and then cattle, sheep, pigs, and horses.  These then were dispersed, along with agriculture, into Europe and North Africa. Alpaca and llamas were domesticated in South America, chickens in southeast Asia, and, again, many more over time.  

How is all this known?  In part, molecular genetics has revealed some of the relationships between wild and domesticated forms of each of these plants and animals, but for animals, bones found at early Neolithic settlement sites have told much of the tale.  However, the tale they tell isn't always clear -- it was thought early on that size of the animals indicated domestication, until archaeologists realized that all animals had gotten smaller through the Paleolithic, including humans.  And, sex and age of animals in piles near settlements was thought to be a sign, if the animals were primarily female, and the males were young, until it was realized that this demographic profile could just as credibly indicate that the males had been hunted.  And so on.  

Teosinte to maize

The only way paleoanthropologists can interpret what they find is through a contemporary lens.  E.g., we know that males aren't of use to a modern dairy farmer so probably weren't to Neolithic farmers either, which could explain the predominance of female sheep or goats in piles of bones.  Many animals did get smaller when domesticated, so size could legitimately be a signature of domestication.  For some grains, the primary difference between wild and domesticated forms are that the seeds of the domesticate don't 'shatter', or fall to the ground when blown by a breeze or brushed by an animal, or when the grain is harvested. But domesticated grains lose the shattering trait, and that's a huge advantage when it comes to harvesting and storing the grain.  

Teosinte and maize;  Nicolle Rager Fuller, National Science Foundation

Corn is another matter.  The wild form of maize is teosinte, which was domesticated about 9000 years ago.  But, teosinte doesn't look much like maize.  It has many branches, it's not as tall, it has tiny ears, the seeds are encased in hard nut-like shells and, unlike maize, they mature serially rather than simultaneously.  Molecular comparison of the genomes of modern wild teosinte and domesticated maize show basically five genetic differences between the plants, and these are responsible for the transition from teosinte to corn.  

But still, the question was why was this plant a candidate for domestication at all, given its less than ideal characteristics for farming? And even for foraging, if the seeds from this scrappy plant didn't ripen all at once, and the shells were difficult to open.  Early farmers couldn't see into the plant's future, weren't thinking ahead to a maizeier form of the plant.  Presumably they were just planting the seeds, assuming they'd get more of the same.  So why try domesticating it?  

Well, it turns out that modern teosinte may not be what teosinte looked like 10,000 years ago, when the temperature was 3-4 degrees lower than it is now, and there was less carbon dioxide in the atmosphere.  Anthropologist Dolores Piperno and colleagues published a paper in Quaternary International last year reporting a an experiment with teosinte that might be the explanation.  They decided to grow teosinte in a greenhouse under early Neolithic environmental conditions, so the built a greenhouse and supplied teosinte plants with the growing conditions they assumed were true at the beginning of the Neolithic.  And they found that even with the same genome that now builds a leggy, short plant with lots of tiny cobs and nut-like kernels, changing growing conditions produced plants that were in fact maizier. 

The plants had a single tall stem, the ears were topped with the tassels we’re familiar with from modern corn, and they had a few short branches with ears, and seeds that matured all at once rather than sequentially. The seeds were exposed, too, rather than encased in the hard seedcase.  With fewer branches, and seeds that were easily visible, all maturing at once, teosinte would have been much easier to harvest for early Neolithic farmers, and it might not have been such a leap to produce maize.     

Complicating evolutionary just-so stories

If Piperno and her coauthors are right, this means that modern versions of wild plants don't necessarily represent their ancestral selves.  The reason for this, they suggest, is ‘phenotypic plasticity,’ which is characteristic of many organisms as they respond to different environmental conditions with changes in appearance.  

Phenotypic plasticity: Pines in California mountains. (Top) At high altitude they hunker downlike bushes. (Bottom). Lower down, these trees are . . . trees. Pictures by John Muir, from Muir, 1894

The teosinte story is a cautionary tale for several reasons.  While molecular data confirm that teosinte is the mother of maize, and that part of the story isn't in doubt, it should be a reminder that evolutionary Just-so stories told from our vantage point today may be skewed.  This is true for archaeology but the moral -- we may not have all the data -- applies just as well to all other sciences.  And probably equally to life in general.  

It's also important because phenotypic plasticity is the norm, which makes evolutionary sense since environments frequently change, and organisms that can't adapt may well be doomed.  But, adaptive stories are so tempting.  

The Wars Within

Life is an ecology at all levels, from the biosphere itself (sometimes referred to as 'Gaia') to the rumbling that goes on inside you as you and parasites who want to eat you from the inside out, struggle for supremacy.  Ultimately nobody wins, as these are age-old struggles.  But there are different strategies for at least winning battles.

Different stages in the life cycle require different levels of resource allocation.  Thus, according to a new paper in The American Naturalist, Competition and the Evolution of Reproductive Restraint in Malaria Parasites, by Pollitt et al., the trade-off in resource allocation between more and less costly life stages is a "key problem for natural selection to solve."

CDC image, Wikimedia Commons.  Parasite life cycle describe here.

To address this issue, Pollitt et al. look at the life stages of malarial parasites to propose a solution to the problem of how evolution decides to most efficiently divide resources between different life-history stages.  The work is described on the BBC website here.  They have a particular interest in the inter-parasite dynamics in the bloodstream of an infected organism.

For malaria parasites, in-host replication and between-host transmission are two distinct stages of the life cycle.  How, Pollitt et al. wonder, does evolution solve the problem of how to allocate resources between these two stages?

This is analogous to the trade-off between reproduction and maintenance faced by multicellular sexually reproducing organisms.  The assumption that reproduction is costly, resulting in tradeoffs between reproduction and survival and between current and future reproductive effort, is a key concept in evolutionary biology.

And, they say that, in spite of the toll malarial infection takes around the world, little is known about the investment strategies of malaria parasites, although they seem to invest "remarkably little" in transmission during infection. But, many infections are by a genetically heterogeneous mix of parasites, and in-host competition for resources between the different infecting genotypes seems to lead to reproductive constraint.  

Previous studies suggest that when in-host survival is threatened parasites increase investment in between-host transmission at the expense of in-host replication but recent evolutionary theory predicts that the opposite should occur.

The recent discovery that malaria parasites can detect and respond to the presence of unrelated competitors suggests that they could also use this information to decide how much to invest in reproduction. [By the way, see the publication for references; it's chock full.]

First, we used a bank of genotypes to test for genetic variation in patterns of gametocyte investment throughout infections. Second, we monitored three focal genotypes in single and mixed infections with one or more competitors to test whether investment in gametocytes is facultatively reduced in competition. Third, we predicted that if reproductive restraint in mixed infections enables parasites to gain the greatest share of exploitable resources, then the investment decisions of each genotype will be influenced by the availability of these resources.

They infected mice with various parasites, and assayed the parasite load and life cycle stages.  And, they calculated the 'gametocyte conversion rate', the proportion of parasites that differentiate into sexual stages relative to asexual stages, relative to genetic mix of an infection, which is their measure of the extent of competition a parasite is facing.

They found "significant genetic variation and phenotypic plasticity in the reproductive effort of malaria parasites."  And, that, in the context of mixed infections, investment in gametocytes is reduced, and diverted into asexual replication.  That is, competition reduces investment in reproduction.  Pollitt et al. suggest that they do this by taking the measure of their environment and responding accordingly.  But, this brings up the question of how they know that they are in the midst of a heterogeneous infection.  What alerts them to the fact that they aren't surrounded only by kin?  And if it really does matter to them, are we verging on a 'group selection' scenario?  And in that sense, isn't cooperation as important here as possible competition?

Parasites inside you are attacked on their own microscopic level.  We described some of this at length in our book The Mermaid's Tale.  Big organisms like us have immune systems to recognize invaders by their surface-molecular characteristics, and we do this by generating molecules of all sorts of which one, at least, will 'recognize' the invader, bind to it, and trigger a destructive reaction.  But the parasites don't like this, and when we've got too good a hold onto their characteristics, they have gene families coding for cell-surface proteins (called var or avr genes in some species), from which they can randomly pick a different gene to express on their surfaces, which makes them again invisible until the immune system regroups and goes at it anew.

If the results reported in this paper hold up, we think they suggest more about adaptability and facultativeness than any generality about natural selection's problem solving abilities.