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April 25, 2007

Bigger males, or smaller females?

As you may have noticed, males and females look different in many species. In “brood parasite� cuckoos, those members of the cuckoo family that lay their eggs in nests of other "host" species, males are mostly bigger and more colorful than females. Did males become bigger and more colorful over the course of evolution? This could be due to sexual selection, based on female choice or conflict between males. Or, did females become smaller and less colorful? That could be due to coevolution with the host species. Less colorful females are less likely to be noticed hanging around host nests, and smaller females may lay smaller eggs that are harder for hosts to tell from their own eggs.

This week’s paper is “The evolution of sexual dimorphism in parasitic cuckoos: sexual selection or coevolution?� by O. Kruger and colleagues at the University of Cambridge and Boston University, published online in Proceedings of the Royal Society.

Kruger and colleagues looked at all 141 cuckoo species. Some care for their own young; others are parasitic. Two authors independently scored each species for male versus female differences in appearance. Wing length was used to see which sex was bigger in each species.

They then compared these data to the cuckoo phylogeny (family tree). It was already known that brood parasitism has evolved three times. Further evolution within the three parasitic branches led to a total of 59 parasitic species, almost half of all cuckoo species.

They used a computer program that combines family trees with data on living species to infer the mostly likely traits of ancestral species at each branch of the tree. This showed how traits changed along each branch.

In cuckoos that raise their own young, 71% of species have females larger than males -- eggs cost more than sperm -- whereas 84% of parasitic species have males larger than females. Compared to their nonparasitic ancestors, two branches showed a change towards males being larger than females. In the third branch, males were already bigger, but this difference increased. Statistical analyses linked to the family tree suggest that these trends were mainly due to a decrease in size for both sexes, with females decreasing more than males.

Evolution of color differences was less consistent. In two of three parasitic branches, plumage changed from “showy� to “cryptic� in both sexes, but the third branch became more showy. The showy species trick hosts into chasing them, then sneak back to the nest and lay eggs.

Coevolution of traits linked to parasitism was a better explanation for evolutionary trends in sex differences than was sexual selection based on female preference or competition among males.

But is there still some role for sexual selection? If females that mate with smaller males have smaller daughters, and those daughters are less likely to have their eggs detected and thrown out of host nests, have females evolved a preference for smaller mates? If so, how does female preference interact with conflict between males differing in size? As we scientists like to say, more research is needed.

Other interesting papers in the same issue:

Although some female preferences based on male appearance may be arbitrary, another paper shows that colorful sexual ornaments in stickleback fish are a good predictor of whether the male has enough carotenoids for a long and healthy life, a trait he might pass to his sons. "Why do men marry and why do they stray?" looks at the timing of male infidelity in one foraging and farming culture with <10% polygamy and concludes that men marry to maximize resource provisioning to their children, not to monopolize "access to women's fertility." Meanwhile, back at Meercat Manor, subordinate males, who we thought were stuck home baby-sitting, may father up to 25% of babies in nearby groups. Are fundamentalists right that evolution leads to sex? It certainly did here, but it's risky to generalize from only one planet.

April 19, 2007

This year in intelligent design

There are hundreds of papers published each month whose authors find evolution useful in explaining their results. One would think that, if "intelligent design" has any scientific merit, there would be a significant number of papers each month presenting evidence of supernatural intervention by an intelligent designer. Surely the many religious scientists, in particular, wouldn't fail to publish results that turn out to support intelligent design, even if that wasn't the original focus of their research.

However, I haven't seen even one paper on intelligent design so far this year that meets the basic scientific criteria in my first post. Maybe I've missed some? Let's check the Discovery Institute web site.

No, nothing so far in 2007. What about 2006?

Aha! Here's one by Ø. A. Voie, "Biological function and the genetic code are interdependent," Chaos, Solitons and Fractals, Vol 28(4) (2006): 1000-1004.

Despite the weird title, this is a real journal. They're not likely to have any biologists among their peer-reviewers, but at least it's a journal. How about my requirement that papers of the week contain new data? Oh, too bad. It's just a bunch of incoherent philosophizing.

Anything else for 2006? No, that's it.

If I had a senior grad student publishing as little as the entire "intelligent design" community put together, I would be suggesting that he or she reconsider whether a career in science makes sense for someone unlikely to be competitive for grants in today's tight-funding environment.

But wait, I missed an article on intelligent design published in 2007! No new data in this one either, but at least the discussion is based on papers with lots of data. Also, it's a book chapter, so peer review was probably less stringent than we'd expect with a good journal. Still, how could the Discovery Institute have missed this one?

Maybe because it's about intelligent design of crops by humans. Disclosure: I wrote it. The topic is closely related to our previous work on Darwinian Agriculture. If the link disappears, here's the citation:
Denison, R.F. 2007. When can intelligent design of crops by humans outperform natural selection? p. 287-302. In: Spiertz, J.H.J., P.C. Struik, and H.H. van Laar (eds.). Scale and complexity in plant systems research: gene-plant-crop relations. Springer.

If the Discovery Institute adds this to their list, can I sue for libel?

Next week: back to peer-reviewed journal articles with original data. They've been piling up.

April 17, 2007

Darwinian agriculture II

Last week, I was at a meeting in the Netherlands on "Darwinian agriculture: the evolutionary ecology of agricultural symbiosis." Topics included: the effects of cows on human evolution, the independent invention of "agriculture" by ants and termites, and some disadvantages of diversity. As promised, here are a few highlights.

Dan Bradley (Ireland) discussed the evolution of cows since domestication by humans. How closely related are cows to the extinct wild aurochs? In other words, how recently did they share a common ancestor? In other words, how long have humans limited interbreeding between wild aurochs and the animals they raised for milk and meat? (Limiting interbreeding allows two groups to evolve differences, as discussed previously for fish.) Different methods, both based on DNA from old auroch bones and cows, give different answers. When they compared mitochondrial DNA (inherited only from mothers) they estimated that cows and aurochs last interbred about 10,000 years ago. So humans domesticated aurochs around the same time as crops like wheat. But comparing Y chromosomes (inherited only from fathers) suggests much more recent crossing. Which is right? Probably both. If an aurochs bull sneaked into a field and mated with a cow, the calf would be raised as part of a farmer's herd. But calves from reverse matings stayed with their wild aurochs mother. Similar patterns are seen in some human populations. For example, in the British Isles, Viking Y chromosomes are more common than Viking mitochondria.

Apart from the occasional auroch raid, humans have controlled the evolution of cows for thousands of years. But cows have influenced our evolution, too. Albano Beja-Pereira (Portugal) mapped the distribution of lactose tolerance in humans. Other mammals (except house cats) can't digest this milk sugar as adults. In Europe, the ability to digest lactose is concentrated in northern Europe, centered on Denmark. People in this region have been using cows to convert grass into meat and milk for thousands of years. If you have only one cow, the choice between meat for a few days or milk for months seems pretty clear. Among humans who raised cows, the few who didn't lose the ability to digest milk as they got older were more likely to survive and reproduce, so the frequency of lactose tolerance increased over generations. A similar genetic pattern has been seen in some Africans whose ancestors raised cows. Beja-Pereira also looked at genetic variations in cow genes for milk proteins. These genes were more diverse in the same part of Europe where lactose tolerance was most common in humans. This diversity may reflect some combination of deliberate selection (choosing which cows and bulls to breed) and the evolutionary effects of larger cow populations in this region.

Mike Jeger (UK) explained how computer models of the spread and evolution of pathogens (microbes that cause disease) can help us defend crops. A new fungicide may work for a few years, until mutant fungi resistant to it become common. If we switch to a new fungicide (or some other control method) soon enough, the resistant mutants usually disappear after a few years. There is often some cost of resistance - a fungicide-resistant enzyme may not work as well -- so they can't compete with nonresistant members of their species. But once resistant mutants are common, some may acquire new mutations that reduce the cost of fungicide resistance. After that, we will have to avoid using the fungicide for much longer, before resistant fungi disappear. He also discussed the "evolutionary epidemiology�? of viruses that attack crops. We can breed crops for virus resistance, but some kinds of resistance will be beaten by viral evolution faster than others. With high-value crops, hand removal of plants that show virus symptoms can be practical. Then the only virus strains that survive to the next generation are those that cause disease too mild to be noticed. This approach reminds me of the use of window screens to select for less severe forms of malaria.

The remaining four talks covered various topics, but the effect of diversity was a common theme. Benefits from crop diversity are well known. Disease may spread more slowly in a mixture of two crops than in one-crop "monoculture.�? Mixtures may use soil resources more completely than either crop alone. But all four talks discussed cases where less diversity may actually be better.

Koos Boomsma (Denmark) and Duur Aanen (The Netherlands) discussed ants and termites that depend on fungus "gardens�? for food. In both cases, different insect colonies may grow different strains, or genotypes, of fungi. But each colony grows only one strain. In ant gardens, contact between two different fungal strains triggers a negative reaction that reduces growth. Even manure from ants that ate one strain will trigger this reaction in a second strain. In termite gardens, different fungal strains don't fight. But they don't bond, either, and this also limits growth. Over tens of millions of years, ants and termites have evolved behaviors that maintain their gardens as fungal monocultures. Ants remove alien fungi, even strains that might be grown by another ant colony. Termites prevent their fungi from reproducing sexually, by eating fruiting bodies that could produce sexual spores. Without sex, one strain gradually takes over.

My former student, Toby Kiers (US and Netherlands), talked about how human farming methods affect the evolution of microbes that help crops. Rhizobia are bacteria that provide some crops with nitrogen. Mycorrhizal fungi provide some crops with phosphorus. Both are symbiotic, in long-term physical contact with their plant hosts. If there were only one strain of microbe per plant, plants with better microbes would grow more. Microbes associated with bigger plants would reproduce more. So better microbes would be more common in the next generation. In other words, the microbe populations would evolve greater mutualism. That's what would happen if the microbe population associated with each plant were a monoculture, but it's not. With many strains per plant, a strain that helps the plant indirectly helps its worst competitors. Microbes from the same plant are, after all, most likely to compete for the next host plant. Toby has shown that soybeans, at least, have evolved a defense against bad rhizobia. She kept some rhizobia from giving the plant any nitrogen, as if they were a bad strain. She did this by surrounding the nodules (bumps on the roots that house the rhizobia), with gas lacking nitrogen. The plant shut off oxygen to those nodules, and the rhizobia inside grew less. My last post has an MP3 file describing this work. Toby also compared different soybean varieties, in the field. Some did better with a mixture of good and bad rhizobia than others, perhaps due to differences in the "sanctions�? they impose on bad rhizobia. Sanctions against nodules that don't supply nitrogen may solve the problem of too much rhizobium diversity within a plant. Diversity within a nodule may still be a problem, though. We don't think the plant can impose sanctions on some rhizobia within a nodule without hurting them all.

Finally, I talked about breeding crops that yield more per acre (or hectare) because individual plants compete less with each other. The best-known example is plant height. Short plants make more grain because they waste less on stems. This works well if you have a whole field of short plants. But, in a mixture, the taller, low-yield plants shade out the shorter high-yield plants. Plants that branch less can yield more, in monoculture, but can't compete against plants that branch more.

I discussed similar tradeoffs, especially for roots in a previous post. At the meeting, Hans de Kroon questioned the paper I cited on wasteful aggression among roots. Two plants sharing a large pot may grow more roots, relative to each plant would in a pot half the size, just because they make more roots in a bigger pot, not because of root interactions. Breeding for less root is probably still a good idea, but root interactions may not be the key.

Whether we look at ant or termite fungus gardens, microbes that help crops, or crops themselves, diversity can lead to interactions that reduce growth. Should we work to reduce diversity in agriculture, then? Not exactly. Diversity may be useful at some scales, but harmful at others. If the world grew more different crops, a disease that killed any one crop would have less effect. But that may not mean that every field should contain more than one crop. We may also benefit by growing different crops in a field in different years, the well-known practice of crop rotation.

Shortly after returning from the meeting, I got a notice for another meeting on "Plant breeding for organic and sustainable, low-input agriculture." I agree that organic farmers need cultivars that are competitive with weeds. I hope speakers at this planned meeting will recognize the tradeoffs between competitiveness and yield, discussed in previous entries and in our paper on Darwinian Agriculture. For a farmer, higher prices for organic products may balance lower yields. But lower yields require using more land to grow the same amount of food, perhaps draining wetlands or clearing forests. Population growth and using crops to make ethanol put still more strain on food supply, raising prices and increasing demand for land to farm.

Related papers by the speakers:

Beja-Pereira A., G. Luikart, P. R. England, D. G. Bradley, O. C. Jann, G. Bertorelle, A. T. Chamberlain, T. P. Nunes, S. Metodiev, N. Ferrand, and G. Erhardt. 2003. Gene-culture coevolution between cattle milk protein genes and human lactase genes. Nature Genetics 35:311-313.

Denison R. F., E. T. Kiers, and S. A. West. 2003. Darwinian agriculture: when can humans find solutions beyond the reach of natural selection? Quarterly Review of Biology 78:145-168.

Gotherstrom A., C. Anderung, L. Hellborg, R. Elburg, C. Smith, D. G. Bradley, and H. Ellegren. 2005. Cattle domestication in the Near East was followed by hybridization with aurochs bulls in Europe. Proceedings of the Royal Society B 272:2345-2350.

Hess K. and H. de Kroon. 2007. Effects of rooting volume and nutrient availability as an alternative explanation for root self/non-self discrimination. Journal of Ecology 95:241-251.

Jeger M. J., S. E. Seal, and F. Van den Bosch. 2006. Evolutionary epidemiology of plant virus disease. Advances in Virus Research 67:163-203.

Kiers E. T., S. A. West, and R. F. Denison. 2002. Mediating mutualisms: farm management practices and evolutionary changes in symbiont co-operation. Journal of Applied Ecology 39:745-754.

Kiers E. T., R. A. Rousseau, S. A. West, and R. F. Denison. 2003. Host sanctions and the legume-rhizobium mutualism. Nature 425:78-81.

Poulsen M., J. J. Boomsma. 2005. Mutualistic Fungi Control Crop Diversity in Fungus-Growing Ants. Science 307:741-744.

April 9, 2007

Evolutionary sound bites

There's an interesting discussion at Pharyngula and The Loom about the challenges of communicating science to nonscientists.

When I suspect an interviewer's only going to use a sound-bite, I decide in advance on a few I wouldn't mind them using. This doesn't always work, though. NBC interviewed me about transgenic crops a few years ago. They kept asking "can consumers tell if food is transgenic?" They already knew the answer and apparently had a script calling for a scientist to say "no" on camera. You might think they would want to talk to experts before deciding what the important questions are, but apparently not. So I kept saying, "that's not the issue; the question is how growing these crops will affect the evolution of weeds and insect pests." Not a bad sound bite, in my opinion, but it wasn't in their script. So they ended up just using visuals from my research fields, and adding their own stupid narration. Maybe if I'd said, "no, and labeling won't help" I would have had a chance to explain about gene flow, but I doubt it.

In contrast to my NBC experience, here's a nice example of telling a complex science story in 90 seconds. It's about our research on the evolution of cooperation between rhizobium bacteria and plants.
Download MP3 file

I like the sound bite, "an evolutionary effect, changing the proportion of good vs. bad rhizobia in the next generation." Evolution is a change in the genetic composition of populations, not "frogs suddenly turning into cows." Staff at the American Association for the Advancement of Science produced this story for their radio program, Science Update, which was nice of them, since we published the work with their main rival. They only got one detail wrong: rhizobia could get plenty of oxygen outside in the soil, so they enter root nodules mainly to get carbohydrates. But, once inside, the plant controls their oxygen supply, as described in the story.

I've also been impressed with the audio version of Science News, especially biology stories by Susan Milius. Like the AAAS radio spots, they're short, but still much longer than the sound-bites typical of commercial radio or TV.

My least favorite evolutionary bumper sticker is "evolve or die." We're all going to die, however our species evolves. I kind of like "stop evolution now", though.

According to the Fog index (which I learned about from Postgenomic), I should use shorter sentences and shorter words. I'll try.

April 6, 2007

Darwinian agriculture I

Next week, I'm speaking at a one-day symposium on "Darwinian Agriculture: the evolutionary ecology of agricultural symbiosis", in Wageningen, The Netherlands. So, instead of reviewing a recent paper, this week I'm going to discuss some of the not-quite-so-recent papers on which my talk will be based. The following week, I plan to summarize some of the talks I hear at the meeting.

I may do the same thing in August, when my grad students and I speak at the much larger Ecological Society of America meetings in San Jose, California. Feel free to comment if you feel cheated of your weekly paper review, and I might reconsider. The Evolution meetings are in Christchurch, New Zealand, this year, but my grant won't stretch that far.

"Darwinian Agriculture: when can humans find solutions beyond the reach of natural selection?" was the title of a paper that Toby Kiers, Stuart West, and I published in 2003. Our answers to the title question suggested how increased understanding of past and ongoing evolution could improve: 1) breeding of crops and livestock, and 2) design of agricultural ecosystems.

With respect to genetic improvement of crop plants, we wrote:

"most simple, tradeoff-free options to increase competitiveness (e.g., increased gene expression, or minor modifications of existing plant genes) have already been tested by natural selection. Further genetic improvement of crop yield potential over the next decade will mainly involve tradeoffs, either between fitness in past versus present environments, or between individual competitiveness and the collective performance of plant communities."

Since then, every time I give a talk on this subject, I look for papers that might disprove this tradeoff hypothesis. I also look for examples of tradeoffs that were rejected by natural selection, but which might be acceptable in agriculture. For example, many people are working on improving drought tolerance of crops. Is it possible to improve on natural selection for this trait?

In 2004, Capell et al. reported that "Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress" (Proc. Nat. Acad. Sci. 101: 9909). Sounds good, but what about the data? They reported "drought-induced rolling of leaves" in control plants, but not in their transgenic plants. Leaf rolling reduces solar heat gain by leaves and may help plants survive until it rains, so it's not clear that losing this trait is an improvement. The transgenic plants apparently "had a slightly decreased growth rate and flowered 4-5 days later" although there was enough variability that they couldn't be 95% sure of this. How did the combination of reduced leaf rolling, slower growth, and later flowering affect grain yield under drought in the field? What about yields in wetter years? Apparently they didn't measure yield, even in a greenhouse. I predict that, under field conditions, the transgenic plants will have lower yield than their nontransgenic parents, at least in normal years. (Otherwise, plants with a modified polyamine pathway trait would already have displaced "normal" competitors.) I don't want to guess, either way, about yields under drought.

In 2005, Park et al. reported (Proc. Nat. Acad. Sci. 102:18830) that transgenic tomato plants, which were genetically engineered to over-express an ion pump gene, grew more roots. This let them take up more water (from soil in pots in a greenhouse), so that they wilted less than nontransgenic tomatoes when the pots weren't watered for 5 days. OK, but is there likely to be any water in the soil during drought, under field conditions, at the depths where the extra roots form? And what about the carbon cost of making more roots? Would investing that carbon in more leaves (which bring in still more carbon, through photosynthesis), rather than more root, perhaps contribute more to tomato fruit yield? The answer to this question might depend on whether the tomatoes are irrigated and, if not, whether the year is wet or dry. I would be surprised if these transgenic tomatoes turn out to yield more than existing cultivars, especially with irrigation or normal rainfall.

So far, I don't see any reason to believe that further increases in the ability of individual plants to survive drought (a trait that natural selection has been working on for millions of years) will lead to much improvement in crop yield over a useful range of field conditions. But are there drought-related traits that would have been eliminated by past natural selection, but which would nonetheless be useful in agriculture?

Maybe. Mathematical modeling (Field Crops Research 61:179) suggests that natural selection results in plants that make too much root for their own (collective) good. From a farmer's point of view, crops should make just enough root to take up the available water, because any resources used to make extra root are resources not available to make tomatoes or beans. But natural selection has favored aggressive rooting, in which each plant "steals" as much water as possible from neighboring plants.

How could we modify this behavior? We could simply breed for less root, not more, but maybe we can do better than that. Surprising recent research suggests that plant roots respond to nearby roots in a way that discriminates between a plant's own roots and those of a neighbor (Proc. Natl. Acad. Sci. 101:3863). The resulting below-ground aggression appears to have a significant cost in reduced seed production (Plant Ecol. 160:235). Modifying root-root interaction genes so that plants "love their neighbors as themselves" might therefore optimize root growth, at the level of the whole crop, over a wide range of conditions. [Update: this might not be the best approach. See Darwinian Agriculture II.]

In effect, this would be selecting for group-level benefits, reversing the effects of past natural selection for individual competitiveness. A similar approach has already been successful in breeding laying hens. Selecting which hens to use for breeding, based on the egg production of a group of hens rather than individuals, led to less aggression among hens and greater collective egg production (Poultry Sci. 75:294).

I guess I will leave an evolutionary perspective on the design of agricultural ecosystems for another post. Any curious and impatient readers can look up our 2003 paper.