Tag Archives: Red Queen

In flour beetles, coevolution mixes things up

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A red flour beetle. Photo via Wikimedia Commons.

Cross-posted from Nothing in Biology Makes Sense.

ResearchBlogging.orgWhen evolutionary biologists think about sex, we often think of parasites, too. That’s not because we’re paranoid about sexually transmitted infections—though I’d like to think that biologists are more rigorous users of safer sex practices than the general population. It’s because coevolution with parasites is thought to be a major evolutionary reason for sexual reproduction.

This is the Red Queen hypothesis, named for the character in Lewis Carroll’s Through the Looking Glass who declares that “it takes all the running you can do to keep in the same place.” Parasite populations are constantly evolving new ways to infest and infect their hosts, the thinking goes. This means that a host individual who mixes her genes with another member of her species is more likely to give birth to offspring that carry new combinations of anti-parasite genes.

But although sex is the, er, sexiest prediction of the Red Queen, it’s not the whole story. What matters to the Red Queen is mixing up genetic material—and there’s more to that than the act of making the beast with two genomes. For instance, in the course of meiosis, the process by which sex cells are formed, chromosomes carrying different alleles for the same genes can “cross over,” breaking up and re-assembling new combinations of those genes. Recombination like this can re-mix the genes of species that reproduce mostly without sex; and the Red Queen implies that coevolution should favor higher rates of recombination even in sexual species.

That’s the case for the red flour beetle, the subject of a study just released online by the open-access journal BMC Evolutionary Biology. In an coevolutionary experiment that pits this worldwide household pest against deadly parasites, the authors show that parasites prompt higher rates of recombination in the beetles, just as the Red Queen predicts.

The red flour beetle, Tribolium castanaeum, is named for its predilection for stored grain products. This food preference makes the tiny beetles particularly easy to raise in the lab, where they’ve been useful enough as a study organism to rate a genome project, which was completed in 2008.

Another red flour beetle. Photo via Icelandic Institute of Natural History.

Tribolium castanaeum reproduces strictly sexually. But, like any other biological trait or process, the beetle’s rate of recombination can vary, and evolve. And, as I’ve explained above, the Red Queen suggests that selection by parasites should favor higher rates of recombination. So the authors of the new study set experimental populations of the beetle to evolve either in parasite-free habitats, or under attack by Nosema whitei, a protozoan that infects and kills flour beetle larvae.

The team started experimental populations of beetles (fed on organic flour, natch) in each of the two treatments with eight different genetic lines, maintaining them at a constant population by collecting 500 beetles at the end of each generation to start the next generation. To make the coevolution treatment coevolutionary, the authors also transferred spores of the parasite produced in the previous generation to infect each new generation of beetles.

After 11 generations of coevolution, the authors sampled male beetles from four of the experimental populations in each treatment, and mated them with females from the same genetic line. By collecting the genotypes of the sampled males for a small number of strategically chosen genes, and comparing them to the genotypes of the males’ offspring, it was then possible to identify recombination events—offspring who had combinations of alleles at different genes that weren’t seen in their fathers.

And, indeed, the frequency of recombination—the proportion of offspring whose genetics showed signs of recombination events when compared to their fathers—was greater in the experimental lines that coevolved with Nosema whitei.

That’s a fairly remarkable result for a simple, relatively short selection experiment, and to my knowledge it’s the first of its kind to deal with recombination, as opposed to sex. There are a few study systems in which natural populations show signs of coping with parasites by having more sex, including C.J.’s favorite mollusks, and there is one good experimental example in which the worm Caenorhabditis elegans evolved to reproduce sexually when confronted with bacterial parasites. But this study marks a new bit of empirical support for the Red Queen: coevolution acting to boost the gene-mixing benefits of sex. ◼

References

Kerstes, N., Berenos, C., Schmid-Hempel, P., & Wegner, K. (2012). Antagonistic experimental coevolution with a parasite increases host recombination frequency BMC Evolutionary Biology, 12 (1) DOI: 10.1186/1471-2148-12-18

Morran, L., Schmidt, O., Gelarden, I., Parrish, R., & Lively, C. (2011). Running with the Red Queen: Host-parasite coevolution selects for biparental sex. Science, 333 (6039), 216-218 DOI: 10.1126/science.1206360

Nothing in Biology Makes Sense: Making sense of sex

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Host-parasite coevolution is like a box of chocolates … Photo by HAMACHI!.

I’m not a particularly big fan of Valentine’s Day, but Nothing in Biology Makes Sense! contributor C.J. Jenkins really, really is. She’s marking the day with chocolate, red wine, and a new mathematical model explaining the evolution of sex:

There have been a number of different mechanisms of selection that have been proposed to explain sex: host-parasite interactions (Bell 1982), elimination of deleterious alleles (Mueller 1964), and various forms of selection (Charlesworth 1993; Otto and Barton 2001; Roze and Barton 2006). However, none of these alone are able to theoretically overcome the two-fold cost of producing males, so many biologists have started taking a pluralist approach (West et al. 1999; Howard and Lively 1994) and combing one or more of the advantages to being sexual in an effort to understand why the birds do it, the bees do it, and even educated fleas do it.

To learn how a new study revives the longstanding “Red Queen” theory—that sex is beneficial because sexually-produced offspring are more likely to carry genes that can help fight off parasites—go read the whole thing. ◼

The joy of sex (well, one, anyway): Fewer parasites

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Natural selection does not necessarily love sex. Photo by xcode.

Hey, don’t knock [selfing]! It’s sex with someone I love.
—Woody Allen, in Annie Hall

Sex is a puzzle to evolutionary biologists. I don’t mean that we’re socially awkward—I mean that sexual reproduction, which involves mixing your genes with someone else’s to produce one or more children, seems to be at odds with natural selection. Every child produced by sexual reproduction carries only half the genetic material of each of her parents; but parents who can make children without sex pass on all their genes to every child.

Over time, individuals who can make babies without sex should become more common in the population than individuals who have to have sex to reproduce, simply because every baby produced without sex “counts” twice as much for its parent. We know of cases (for instance, stick insects) where asexual reproduction has apparently evolved and spread multiple times.

And yet, not only is sexual reproduction widespread in the natural world, there are many species of living things in which some individuals reproduce sexually and some reproduce without sex, and the two types coexist more-or-less stably. This is particularly common in plants, but it’s also seen in lots of other taxa. That suggests there must be something useful about sexual reproduction that offsets the cost associated with making only half a copy of your genome for every child you have.

One popular hypothesis is that sexual reproduction helps generate new combinations of genes to fight parasites and diseases—this is called the Red Queen Hypothesis, after the character in Through the Looking-Glass who tells Alice that “… it takes all the running you can do, to keep in the same place.” Sex, the thinking goes, means that your children are more likely to have new parasite-fighting gene combinations, and that populations can “run faster” in the coevolutionary race against parasites. And now, a new study in a population of peculiar little fish provides some reasonably direct evidence [$a] for that proposed benefit of sex.

A mangrove killifish. Photo via USGS, used under fair use rationale.

The mangrove killifish, Rivulus marmoratus, leads a pretty remarkable life even before you consider its reproductive strategy. Mangrove killifish live in coastal mangrove swamps, where they must contend with changes in water salinity and water level—and they deal with dry spells by packing into hollows in mangrove tree trunks. Jammed together in a hollow log, the killifish can survive up to two months entirely out of water.

They’re also one of very few vertebrate species known to be able to reproduce asexually. Most mangrove killifish are hermaphrodites, capable of making both eggs and sperm and combining them—or “selfing”—to lay fertilized eggs. A few killifish develop as “pure” males instead, capable of producing only sperm, and therefore only capable of sexual reproduction. Why that small fraction of males persists in killifish populations is probably related to the selective costs and benefits of sex, both for mangrove killifish and for living things in general.

The Red Queen hypothesis predicts that sex is beneficial because it creates new combinations of genes, which in turn lead to greater parasite resistance. Therefore, if killifish produced by sexual reproduction should have more diverse genomes, and are better able to resist parasites than killifish who only have one hermaphroditic parent, then the Red Queen may be the reason why male killifish haven’t gone the way of the dodo.

This is what Amy Ellison and her coauthors found in a population of mangrove killifish from four sites in Belize. They collected killifish and took their genetic fingerprints to identify individuals that were most likely descended from a single selfing lineage, or those that carried genes from multiple lineages. They also checked each fish for infection by three major groups of parasites—bacteria, a common protozoan parasite of killifish, and parasitic worms.

Their total sample size is a bit small, but the team found a pattern generally quite consistent with the Red Queen. Fish descended from sexually-reproducing parents were more likely to be heterozygous—to carry two different forms of a gene—than fish descended from asexual lines. More importantly, fish descended from sexually-reproducing parents also generally had fewer parasites of all three classes, and were generally less likely to carry any protozoans or worms, than those descended from hermaphrodites. That’s consistent with the Red Queen, and it shows the perfectly good selective “reason” for a hermaphrodite to mate with a “pure” male—even though the hermaphrodite is giving up half the selective benefit of the offspring thus produced, those offspring are more likely to be healthy.

A broader prediction that follows from these results is that mangrove killifish populations with higher rates of parasite attack should have more males, or at least more individuals with two parents. What would really be cool, though, is if hermaphroditic killifish can respond to parasite infections by choosing to reproduce sexually—self-medicating, like monarch butterflies, but with sex instead of a toxic host plant. It’s been observed that the hermaphroditic nematode worm Caenorhabditis elegans responds to environmental stress by giving birth to more male offspring, but I know of no such result in a vertebrate. ◼

Reference

Ellison, A., Cable, J., & Consuegra, S. (2011). Best of both worlds? Association between outcrossing and parasite loads in a selfing fish. Evolution, 65 (10), 3021-6 DOI: 10.1111/j.1558-5646.2011.01354.x

Dethroning the Red Queen?

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ResearchBlogging.orgRegular readers of Denim and Tweed know that I’m fascinated by the evolution of species interactions: interactions between plants and nitrogen-fixing bacteria, Joshua trees and yucca moths, parasitoid wasps and butterflies, and between ants and the trees they guard. I tend to think that coevolutionary interactions not only determine the health of natural populations, but shape their evolutionary history. But would I feel that way if I were a paleontologist?

Running just to stay in place

The idea that interactions between species matter goes all the way back to the origins of evolutionary biology in the writing of Charles Darwin:

What a struggle between the several kinds of trees must here have gone on during long centuries, each annually scattering its seeds by the thousand; what war between insect and insect – between insects, snails, and other animals with birds and beasts of prey – all striving to increase, and all feeding on each other or on the trees or their seeds and seedlings, or on the other plants which first clothed the ground and thus checked the growth of the trees! (On the Origin of Species, 1859: 74-5)

This image of constant struggle among living things was more formally encapsulated in a 1973 paper by Leigh Van Valen (which paper is not, alas, available online), who proposed that constant coevolution with other species should mean that natural populations of living things are constantly adapting – in response to competitors, mutualists, predators, parasites – without gaining ground in the struggle, because the other species are also adapting. Van Valen lifted an image from Lewis Carroll’s Through the Looking-Glass, in which the Red Queen tells Alice that, in the strange world of Looking-Glass Land, “… it takes all the running you can do, to keep in the same place.”

They were running hand in hand, and the Queen went so fast that it was all she could do to keep up with her … The most curious part of the thing was, that the trees and the other things around them never seemed to changed their places at all.


“… it takes all the running you can do, to keep in the same place.” Image from Through the Looking-Glass, via VictorianWeb.

Thus, this idea that fuels much of my research, and a great deal of scientific study over the last three decades, is often identified with the Red Queen. What is interesting about this result is that Van Valen wasn’t interested in species interactions as such; he was trying to explain a pattern in the fossil record – that, for a wide variety of living things, the probability that a species would go extinct was independent of its age. That is, species that have been around for ten million years are no better adapted to their environments than species that have just formed; the probability of extinction is constant.

Van Valen’s explanation for this result was that something must constantly act to prevent living things from becoming better adapted, and better able to resist extinction, over time – specifically, the Red Queen’s race against other living things. Whenever a species “loses” the race, it goes extinct, regardless of how long the race has been up to that point. A similar pattern applies to the creation of new species – if coevolutionary interactions often help create reproductive isolation, then new species should also form at a roughly constant rate [$a]. Since this is what we observe, many biologists conclude that coevolution is responsible for the diversity of life on Earth.

What if the race doesn’t matter?

Fortunately for the advance of knowledge, however, not all evolutionary biologists have the same perspective. Paleontologists, for instance, tend to think that the year-to-year dynamics of the Red Queen race don’t make much difference in the longer run, over millions of years. They’d argue that most of the evolutionary change induced by coevolution between species is too variable and fleeting to have much effect on the rates at which species are formed and go extinct. Under this view, random geological events – continents splitting, mountain ranges rising, volcanoes erupting – are more likely to create new species and force them to extinction.


What matters more in the history of life, the biological environment, or the physical environment? Photos by Martin Heigan and Cedric Favero.

This competing model should also lead to a roughly constant rate of species formation and extinction, but it predicts a different pattern of variation around that constant rate than the coevolutionary Red Queen does. If most speciation and extinction events are caused by coevolution, then the time periods between speciation events should follow a normal distribution – forming a “bell curve” with most periods close to the average length, and symmetrical tails of longer and shorter periods of time. On the other hand, if many different, individually rare geological events are the most common cause of speciation and extinction, the periods between speciation events should follow an exponential distribution, with most periods being shorter than the average, but a long tail of longer periods as well.

This contrast is the crux of a study recently published in Nature. The paper’s authors, Venditti et al., examined 101 evolutionary trees estimated from genetic data, including groups like the dog family, roses, and bees. For each group’s evolutionary tree, they determined the distribution of the lengths of time periods between speciation events. A majority of the trees – 78% – supported the exponential model. That is, 78% of the groups of organisms examined had evolved and diversified in a fashion best explained by geology, not coevolution. None of the groups fit the normal distribution, and only 8% fit the related lognormal distribution.

The Red Queen is dead, long live the Red Queen!

This result suggests that within many groups of organisms, the physical environment is a more common cause of reproductive isolation or extinction than the biological environment. However, this isn’t to say that species interactions don’t matter. As Van Valen originally noted, extinction rates may be roughly constant within large groups of organisms, like those examined by Venditti et al., but those constant rates vary from group to group. These differences in rate may still depend on species interactions, because species interactions can shape how prone a population is to reproductive isolation.

For instance, a group of plants that has lousy seed dispersers may form new species in response to much smaller, and more common, geological barriers than a group of plants whose seeds can travel for hundreds of miles. Additionally, species interactions that promote diversity within the interacting species may mean that when geology creates isolation, the resultant daughter species are more different from each other than they would otherwise be, and less likely to re-merge if they come into contact again. Under that scenario, speciation caused by the physical environment would act to preserve variation [$a] created by the biological environment.

So, perhaps the Red Queen doesn’t operate the way we thought she did, with constant coevolutionary races spinning off new species and killing off others. But that hardly means that Red Queen processes don’t matter in the long run.

References

Benton, M. (2010). Evolutionary biology: New take on the Red Queen. Nature, 463 (7279), 306-7 DOI: 10.1038/463306a

Futuyma, D. (1987). On the role of species in anagenesis. The American Naturalist, 130 (3), 465-73 DOI: 10.1086/284724

Stenseth, N., & Maynard Smith, J. (1984). Coevolution in ecosystems: Red Queen evolution or stasis? Evolution, 38 (4), 870-80 DOI: 10.2307/2408397

Van Valen, L. (1973). A new evolutionary law. Evolutionary Theory, 1 (1), 1-30

Venditti, C., Meade, A., & Pagel, M. (2009). Phylogenies reveal new interpretation of speciation and the Red Queen. Nature, 463 (7279), 349-52 DOI: 10.1038/nature08630