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February 28, 2007

Experimental evolution: play dead or fly away?

Last week's paper discussed trade-offs between seed size and seed number. Many such trade-offs (growth vs. reproduction, more seeds vs. taller stem, etc.) follow directly from conservation of matter or energy, but what about other sorts of trade-offs? It has been suggested, for example, that there is a trade-off between competitiveness and dispersal ability. Why should this be? For seeds, at least, a larger seed gives the seedling a head-start against competitors, but smaller seeds travel farther on the wind.

This week's paper proposes another trade-off, for which the mechanism is less obvious. "Drop or fly? Negative genetic correlation between death-feigning ability and flying ability as alternative anti-predator strategies", was written by Tatunori Ohno and Takahisa Miyatake and published in Proceedings of the Royal Society B (vol. 274, p. 555-560).

Prey that are unable to fight back against predators (using horns or nasty chemicals, for example) can flee or hide. Insects can fly away or drop to the ground and "play dead." It's not that predators necessarily refuse to eat a dead insect, but that insects lying on the ground and not moving are hard to see.

The authors of this paper measured flying ability in adzuki bean beetles and compared that to the length of time they would play dead (or "feign death"). Comparing 21 populations of these beetles from around Japan, they found a strong negative correlation. Good fliers weren't good at playing dead, and vice versa.

What would cause such a negative correlation? One possibility is that good fliers escape from predators, so there is no selection for playing dead. Within a population of slow-flying beetles, on the other hand, those that drop to the ground and feign death long enough for the predator to leave are more likely to survive and reproduce. Under this hypothesis, there is no intrinsic trade-off between flying ability and playing dead. Instead, the apparent trade-off would come from different death-feigning selection regimes for good vs. bad fliers.

This hypothesis is wrong in this case, however. We know because Ohno and Miyatake selectively bred beetles for good vs. bad flying ability and separately for short vs. long immobility when playing dead. They found the same negative relationship seen in the field, even though their laboratory experiments didn't include predators. In only eight generations, they got 40-fold differences in duration of death-feigning. (Who said evolution is always slow?) They concluded that there must be some kind of physiological or behavioral trade-off between flying and feigning death.

They did mention a third possibility, namely genetic linkage. Maybe, in their experimental population, there was a gene for flying well that just happened to be close to a gene for not playing dead. I agree with the authors that this is unlikely. They give various examples showing that more active insects are more likely to flee and less active ones are more likely to hide. They suggest that some chemical signal in the beetles' brains stimulates flying and simultaneously reduces the ability to remain still and feign death. I wonder whether prolonged selection for both flying speed (when fleeing) and length of immobility (when feigning death) could break this link.

Overall conclusions? First, evolutionary biology is increasingly becoming an experimental science. With strong selection, a population can behave very differently in only a few generations. Regarding trade-offs, I would not conclude that every claim of a trade-off between X and Y should be accepted uncritically. Some evolutionary innovations that improve competitiveness might simultaneously improve dispersal, for example. On the other hand, this paper shows that we can identify and quantify trade-offs even when their mechanistic basis has yet to be established.

February 20, 2007

Evolutionary trade-offs: how are soybeans like salmon?

Answer: they're both semelparous (reproduce once, then die), so evolutionary trade-offs between number and size of offspring are expected to be similar.

This week's paper is "Evolutionary aspects of the trade-off between seed size and number in crops" (Field Crops Research 100:125-138) by Victor Sadras. You can read the abstract on the web for free. For the full version, you can pay $30 to download, visit your nearest agricultural research library (in the U.S., often at a state university), or email the author at: My discussion is mostly based on a shorter version presented at the Australian Agronomy Conference.

Demand for grain is increasing, to feed growing human and livestock populations and more recently for ethanol production. Unless those trends are reversed, we will either need to expand the land area used for agriculture or increase grain yields per unit area. Grain yield is the product of plants per area, seeds per plant, and weight per seed. Unfortunately, increasing any one of these (by increasing seeding rate, or through plant breeding) tends to decrease the others.

This paper looks at how natural selection (in the wild ancestors of crop plants and in fish) and plant breeding (especially in maize and sunflower) shape trade-offs between seed number per plant and seed size. The similar patterns in plants and fish show that, as predicted by the relevant aspects of evolutionary theory, we are dealing with fundamental constraints that we are unlikely to change.

The genomes of plants and fish (and other semelparous species) are the legacy of past evolution in which the variants that survived were those that maximized the number of offspring surviving to maturity, subject to two constraints:
1) resources are more abundant some years than others, and
2) for any given level of resources, there is some optimal trade-off between size and number of offspring.

In theory, plants could deal with variation among years by making more seeds in good years, by making bigger seeds in good years, or both. A major point of this paper is that most crop plants respond to good conditions mainly by making more seeds, not bigger seeds. Figure 4 (3 in full version) shows 291% variation in seed number of soybean, but only 43% variation in seed size. Trout showed even greater tendency to vary number of eggs rather than their size. More extensive data for a variety of crops confirm this point in the full paper (Fig. 4).

Why vary number rather than size? Sadras refers to a paper by Smith and Fretwell in American Naturalist, a journal read by more evolutionary biologists than crop scientists. This paper showed that, if the chance of a seed surviving to become an adult plant increases with its size, but with diminishing returns (twice as big is only 50% more likely to survive, for example), then there will be some optimum seed size. Beyond that size, the plant would increase its number of descendants more by making more seeds, rather than larger seeds. Colin Donald (whose papers have greatly influenced my own thinking) came to similar conclusions, based on a clever experiment involving competition between seeds of the same genotype but different size.

Sadras concludes that there has been stabilizing selection for seed size. Does this mean that, once seeds have reached their target size, natural selection would favor cessation of seed growth, even if the plant still had resources available that could be used for additional growth? I don't think so, unless seed survival actually decreases with seed size beyond some limit (e.g., due to pod splitting). Rather, it means that there is strong selection for getting seed number "right", i.e., starting the number of seeds that will use all the available resources in growing to the target weight per seed. This is tricky, because some plant processes that determine eventual seed number occur relatively early in the season. What if the rest of the season turns out to be unusually wet or dry?

Sadras shows that there is indeed a strong relationship between resource availability (as indicated by growth rate) and seed (or fish egg) number (Fig. 1). For barley, wheat, and "prolific maize", seed number is predicted with reasonable accuracy by assuming that seed size can't vary (Fig. 2).

On the other hand, maize limited to one ear per plant was unable to increase seed number enough to use all resources available under ideal conditions, so it departed from theoretical predictions. Sadras points out that, in breeding for maize with only one or two ears, or sunflower with a single head, we have decreased the ability of plants to respond to their environment by varying seed number. (Wild sunflower, and teosinte, the wild ancestor of maize, both have more flowers per plant than their cultivated descendants.) They appear to compensate somewhat, with more variation in seed size, relative to seed number, than crops like wheat or soybean (Fig. 4b in full paper). He also mentions work by Harper showing that variability in seed size increases when variation in seed number is limited surgically.

How will crop scientists use the evolutionary insights in Sadras' paper? One possible follow-up would be to think about how variation in resource availability differs between today's agricultural fields and the past environments that shaped the evolution of crops and their wild ancestors. If water supply, for example, is consistently better in irrigated agriculture, then bet-hedging mechanisms that control seed number might be too conservative. If plants make too few seeds, they may have "extra" resources available during seed-fill. Are current crop genotypes able to use those extra resources to make each seed bigger, or will some resources be wasted?

A more general answer is that any crop scientist with some spare time (often a problem, as decreased funding for agricultural research in many countries has increased workloads) could benefit from reading more about evolutionary trade-offs, especially in plants, but also in other species. Salmon and soybeans are different in many ways, but this paper shows that the similarities can be illuminating.

February 14, 2007

Evolution triumphs over photosynthesis

In general, I don't want to waste time responding to tired old creationist criticisms of evolutionary theory that have already been refuted elsewhere (such as here or here) -- criticisms backed by new data would be another story -- but I do need to address one issue that could undermine my ability to find a paper to discuss each week. Some creationists have suggested that scientists are increasingly rejecting evolution. Actually they've been saying this for a long time. Is my paper pipeline drying up?

As a scientist, my own impression is rather different. The main change I've seen over the last 20 years has been an increase, not in the percent of research biologists who accept the basic principles of evolution (never quite 100%), but rather in the percent of research that explicitly uses those principles in trying to understand life on earth, past and present. In other words, rather than just asking "how does photosynthesis work?", more scientists are now asking questions such as "how many times did this type of photosynthesis evolve, when, how, and why?"

But personal impressions can be misleading, so I went looking for data. I searched Science Citation Index for papers with "evolution" in the title or abstract. That gave a lot of papers on evolution of stars, etc., so I limited the search to papers that had both "evolution" and "species." This leaves out a lot of evolution papers -- for example, some medical researchers are more likely to report the "emergence" of antibiotic resistance (from a hole in the ground, presumably) -- but I'm mainly looking for trends over years. What I found was more than a 100X increase in evolution papers per week, between 1975 and 2005.

Could this just reflect an overall increase in biological research over this period, or maybe an increase in the availability of computer-searchable abstracts? To test these hypotheses, I used papers with "photosynthesis" as a control. Photosynthesis papers increased also, consistent with an overall growth in research, but much less than evolution papers did. Photosynthesis papers outnumbered evolution papers 20:1 in 1975, but by 2005 evolution papers outnumbered photosynthesis papers by more than 2:1. So the scientific importance of evolution is increasing relative to photosynthesis, but both are very active areas of research. I'll have plenty of papers to choose from.


You can also download the JPG file:
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What's new in evolution? Lots!

A member of the audience at a recent Cafe Scientifique on "Understanding Evolution" complained that the speakers spent more time talking about the political battle with fundamentalists who don't want evolution taught in schools -- this is especially a problem in the US and Turkey -- rather than discussing new discoveries in evolutionary biology. The theory of evolution is the cornerstone of biology, in the same sense that the germ theory of disease is a cornerstone of medicine, so I agree that increasing the amount and quality of coverage of evolution is a critical educational goal.

But I also sympathized with the audience member who wanted to hear more about science and less about politics and religion. It's not that hard to find out about new discoveries in evolutionary biology if you have access to a university library or even just a good internet connection. But I liked the name, "This Week in Evolution", and nobody seemed to be using it!

Each week, I plan to discuss a scientific paper that meets the following criteria:
1) published during the previous month;
2) about some aspect of evolution;
3) published after peer review in a journal with a citation impact of at least 1.0 (i.e., no third-tier journals);
4) containing significant amounts of data, not just mathematical modeling or discussion.

I welcome suggestions for papers to discuss, including any that challenge major elements of evolutionary theory, but only those that meet the rather minimalist criteria above. So, for example, if some senile member of the National Academy of Science uses his membership status to bypass peer review and publish a paper in Proceedings of the National Academy claiming (without any data) that space aliens are secretly controlling evolution, I won't bother to discuss that paper. (If he had data, he wouldn't need to bypass peer review!) Good papers are sometimes published without peer review (e.g., in the proceedings of a symposium) or in third-rate journals, but sticking to high-impact journals reduces the chances that I'll get halfway through the paper and find they've made some really obvious error. Mathematical models can provide important insights, as can reviews of existing literature -- I have published both -- but one logical flaw missed by peer review can sometimes make the whole paper useless. Papers containing data, on the other hand, are usually informative even if there turn out to be mistakes in interpretation.

I will assume that readers have background equivalent to a good high school or college biology course. These articles might be appropriate for a freshman seminar, but this isn't a remedial course in elementary principles of evolution. So I will assume some familiarity with terms like "chromosome" and "mutation", and with the evidence that: 1) the earth is billions, not thousands, of years old, 2) all known life on earth is descended from a common ancestor, and 3) complex structures, such as eyes can evolve in a series of small steps, each typically giving a small increase in fitness. Although these statements may conflict with some religious traditions, the evidence for each is now so overwhelming that mainstream religions generally accept them. I suggest that "willing to be convinced by overwhelming evidence" is a reasonable definition of "mainstream."

On the other hand, I don't expect any of the papers I discuss will provide data conclusively disproving the existence of god(s), or even the possibility of occasional miraculous intervention in evolution (e.g., creating the first living cell), although we may get more evidence for nonmiraculous hypotheses. We'll see!

Research in my lab on the evolution of cooperation between bacteria and plants is funded by the National Science Foundation, but anything wrong or offensive in this blog is not their fault. See my Department of Ecology Evolution and Behavior web page for my recent papers and my old UC Davis web page for earlier ones.