Snake-eating opossums have evolved venom-resistant blood

The humble Virginia opossum can shrug off snakebites that would kill larger mammals. (Flicrk, TexasEagle)

If you were going to pick the traits of a single animal to confer on a superhero, you probably wouldn’t pick the Virginia opossum. Possums are ubiquitous, scruffy, ratlike marsupials, their toothy grins giving the not entirely inaccurate impression that they don’t have much going on upstairs. Until recently, the nicest thing I could think to say about them is that they eat a lot of ticks.

Blood-sucking Lyme disease vectors are only a small part of the opossum’s eclectic diet, however. They also eat quite a few poisonous snakes, and this has apparently led them to evolve a trait I could call a superpower without exaggeration: opossum blood is resistant to snake venom.

This curious and useful ability was first documented by J.A. Kilmon in a 1976 paper [$a], in which Kilmon reported field observations and laboratory trials showing that opossums tolerate snakebites without visible ill effect. (If animal experimentation makes you queasy, you might want to go read something else about now. Perhaps a nice post about gerbils?)

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What to wear to Pride (if you’re a huge nerd)

Drift happens, and it’s fabulous. Photo by jby.

After the big gay post came out Tuesday, there was really only one shirt I could wear to the Twin Cities Pride parade. You, too, can have the thrill of explaining the Wright-Fisher model of drift and mutation in front of a gay bar—this design is available for purchase, with your choice of American Apparel shirt colors.

The intelligent homosexual’s guide to natural selection and evolution, with a key to many complicating factors

San Francisco Pride, 2008. (Flickr, ingridtaylar)

This is a cross-posting of my latest contribution to the Scientific American guest blog. Since the original went up at SciAm, P.Z. Myers has pointed out a few more complicating factors. If you read one paper to follow up on what I’ve written here, I’d suggest Nathan Bailey and Marlene Zuk’s excellent 2009 review [PDF], which is posted in PDF format by none other than The Stranger.

June is Pride Month in the United States, and in communities across the country, lesbian, gay, bisexual, and transgendered Americans are celebrating with carnivals, parades, and marches. Pride is a rebuke to the shame and marginalization many LGBT people face growing up, and a celebration of the freedoms we’ve won since the days when our sexual orientations were considered psychological diseases and grounds for harrassment and arrest. It’s also a chance to acknowledge how far we still have to go, and to organize our efforts for a better future.

And, of course, it’s a great big party.

I’m looking forward to celebrating Pride for the first time in my new hometown of Minneapolis this weekend–but as an evolutionary biologist, I suspect I have a perspective on the life and history of sexual minorities that many of my fellow partiers don’t. In spite of the progress that LGBT folks have made, and seem likely to continue to make, towards legal equality, there’s a popular perception that we can never really achieve biological equality. This is because same-sex sexual activity is inherently not reproductive sex. To put it baldly, as the idea is usually expressed, natural selection should be against men who want to have sex with other men–because we aren’t interested in the kind of sex that makes babies. An oft-cited estimate from 1981 is that gay men have about 80 percent fewer children than straight men.

Focusing on the selective benefit or detriment associated with particular human traits and behaviors gets my scientific dander up, because it’s so easy for the discussion to slip from what is “selectively beneficial” to what is “right.” A superficial understanding of what natural selection favors or doesn’t favor is a horrible standard for making moral judgements. A man could leave behind a lot of children by being a thief, a rapist, and a murderer–but only a sociopath would consider that such behavior was justified by high reproductive fitness.

And yet, as an evolutionary biologist, I have to admit that my sexual orientation is a puzzle.

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From the archive: Evolution’s Rainbow

White-throated sparrow Photo by hjhipster.

No new science post this week, because I’m taking my time to put together a (hopefully) particularly good, detailed article for the near future. In the meantime, let me suggest something from the D&T archives for Pride month, in advance of the Diversity in Science carnival in a couple weeks. Specifically, my review of Joan Roughgarden’s survey of sexuality across the animal kingdom, Evolution’s Rainbow:

This interest in the evolutionary context of diversity would eventually become much more personal. In 1998, [Roughgarden] came out as transgendered, taking the name Joan after decades spent establishing her scientific reputation under the name she was given at birth, Jonathan. In addition to the challenges inherent to gender transition, Roughgarden’s expertise intersects with her identity in one awkward question: in a biological world shaped by natural selection, how can we explain the evolution of lesbians, gay men, and transgendered people—individuals who are not interested in sexual activity that passes on their genes?

Roughgarden’s answer was to begin a program of research questioning the dominant way of thinking about sex in an evolutionary context. In 2004, she presented her conclusions comprehensively in the book Evolution’s Rainbow, calling for biologists to re-think they way they understood and described sexual behavior throughout the animal kingdom. As another biologist with an admitted personal interest in the question, I’ve found Evolution’s Rainbow to be a great starting point for thinking about sexuality in an evolutionary context.

For in-depth looks at three examples of “alternative” animal lifestyles and the reception Roughgarden’s ideas met in the broader evolutionary biology community, go read the whole post.

Pesticides and parasites add up to an evolutionary Catch-22

When Daphnia evolve resistance to pesticides, they become more vulnerable to bacterial parasites. Photo by Chantal Wagner.

ResearchBlogging.orgIf you haven’t read Joseph Heller’s classic Catch-22, cancel your plans for next weekend and spend the time with a copy from the nearest library. It’s a hilarious, bracingly bleak satire of military bureaucracy, as epitomized in the titular clause governing when bomber pilots can be grounded for reason of insanity:

There was only one catch and that was Catch-22, which specified that a concern for one’s safety in the face of dangers that were real and immediate was the process of a rational mind. Orr was crazy and could be grounded. All he had to do was ask; and as soon as he did, he would no longer be crazy and would have to fly more missions.

Heller conceived Catch-22 as a product of malicious middle management, but a similar situation crops up in the natural world when living things are under natural selection from conditions that favor contradictory traits. Biologists most commonly call these tradeoffs.

Over the course of evolution, tradeoffs set up “choices” that natural selection must make—a population can adapt to one alternative set of conditions, or another, or settle on a middle ground. A trivial example is that elephants have long ago “chosen” not to fly (Dumbo notwithstanding) in the course of evolving large, un-aerodynamic bodies suitable for massive-scale herbivory. A more relevant example is a new finding that the evolution of pesticide resistance creates vulnerability to parasites [$a].

The US Environmental Protection Agency estimated [PDF] that in 2006 and 2007 (the latest years for which reports are online) we used upwards of five billion pounds of pesticides to kill unwanted plants, insects, fungi, and other organisms worldwide. Once they’re sprayed, we don’t have much control over where pesticides end up—rain runoff takes them into lakes, ponds, and the ocean. In those bodies of water, critters at the base of the food chain are the first to feel the effects—critters like the tiny, translucent crustacean Daphnia magna.

Of course, those critters may be able to evolve resistance to the pesticides contaminating their environment—but that resistance may come at a cost.

Pesticide application, via the most picturesque method available. Photo by Scott Butner.

Anja Coors and Luc De Meester had already found a hint of this cost [$a] in an experiment using a single clonal line of Daphnia, in which Daphnia exposed to both sublethal concentrations of the widely-used insecticide carbaryl and a parasitic bacterium fared much worse than Daphnia exposed to only carbaryl or bacteria.

In the new study, Coors, De Meester, and three collaborators expand on that initial observation by determining whether Daphnia become more vulnerable to parasites as they evolve resistance to carbaryl, and whether this costly evolution could occur in natural populations. The coauthors took samples of Daphnia from natural populations in four separate lakes and exposed them to carbaryl over several generations—then sampled the resultant evolved populations and tested their vulnerability to the bacterium. Compared to Daphnia left unexposed to carbaryl, the evolved populations were more resistant to the pesticide—and were also more badly hurt by bacterial infection.

It’s hard to say how general this particular result is to the many, many other species that, like Daphnia, must cope with pesticides and other pollutants humans have introduced into the environment. Evolution to resist one pesticide leads to lowered resistance to infection in one aquatic crustacean; in other species, facing different chemicals, maybe such costs are different or lesser or nonexistent. But living things are not infinitely pliable as they evolve in response to the many and rapid changes we’re making in the world. To slow the extinction crisis going on around us, we need to avoid trapping other living things in Catch-22.

References

Coors, A., & De Meester, L. (2008). Synergistic, antagonistic and additive effects of multiple stressors: predation threat, parasitism and pesticide exposure in Daphnia magna.Journal of Applied Ecology, 45 (6), 1820-8 DOI: 10.1111/j.1365-2664.2008.01566.x

Jansen, M., Stoks, R., Coors, A., van Doorslaer, W., & de Meester, L. (2011). Collateral damage: Rapid exposure-induced evolution of pesticide resistance leads to increased susceptibility to parasites. Evolution DOI: 10.1111/j.1558-5646.2011.01331.x

When does a beneficial mutation fail to benefit?

Beneficial mutations, according to Hollywood, include the superpowered ability to make San Francisco Bay foggy. Photo via Comics Contiuum.

ResearchBlogging.orgEvery time a cell divides is an opportunity for mutation, creating new genetic variation that may be beneficial, may be harmful, or may make no difference at all. In sexually reproducing species, the fate of a useful new mutation is relatively straightforward. If it overcomes the vicissitudes of genetic drift, the mutation will spread through the population as recombination swaps it into different genetic backgrounds, so that on average the mutation spreads or disappears on its own merits.

In asexual species, though, things are less straightforward. This is because new mutations are stuck with the genetic backgrounds in which they first appear—whether they spread of disappear depends not only on the fitness benefits they might provide, but on how beneficial the variation in the rest of the genome is, too. A new beneficial mutation in an asexual population is like a race car driver who can’t change cars—she might be an ace at the wheel, but if she’s stuck in a Yugo, she’s probably not going to win.

So what happens to a new beneficial mutation in an asexual population is largely dependent on random factors: genetic drift and mutation. That randomness means that in order to know how new useful mutations behave in general, the only robust solution is to watch lots of new useful mutations in lots of otherwise identical populations.

In other words, it’s a question best approached using experimental evolution. That brings us to a study just released in advance of print by the journal Genetics, in which a team headed by Greg Lang uses some clever methods to track the origin and fate of beneficial mutations in yeast.

The first clever thing about the project is that its authors knew in advance where to expect a beneficial mutation. Yeast cells reproduce both sexually and asexually—if the experimental populations are maintained in conditions that keep them reproducing asexually, mutations that turn off the costly cellular machinery necessary for sexual reproduction provide a measurable benefit.

Electron micrograph of budding yeast cells. Image from Microbe World.

By using a strain of yeast engineered to produce fluorescent protein in the course of sexual reproduction, the authors could check for the presence of permanently asexual mutants by taking a sample from the population, prompting it to mate and measuring the sample’s total fluorescence. Lower fluorescence would mean that more cells had lost the ability to reproduce sexually; if samples from a population were to become less and less fluorescent over time, the beneficial mutation would be spreading through the population.

Lang and his coauthors then set up the kind of experiment that you can only do with single-celled critters: they started 592 populations of yeast evolve for 1,000 generations of asexual reproduction. Each population started out from a single genetic strain, so differences between populations started from the same strain were purely due to differences in the random processes of mutation and drift. (The full experimental design used two different strains of yeast, and kept the population size at either 100,000 or 1,000,000 cells, for a total of four treatments.)

You might expect that the loss-of-sex mutation would reliably emerge and spread until it dominated each replicate population. In fact, that only occurred in a small fraction of the replicates. In many more cases, the loss-of-sex mutation showed up and started to spread, but was then overwhelmed by yeast that could still reproduce sexually—presumably because other, more beneficial mutations had arisen elsewhere in the population. This phenomenon, clonal interference, is widely expected to happen in competition among clonal strains.

What determined the success or failure of the loss-of-sex mutation? The authors found a considerable range of variation in the rate at which loss-of-sex strains increased in the experimental populations, suggesting that variation elsewhere in the genome contributed to the fitness of the yeast strain carrying the loss-of-sex mutation. Since every replicate population started as a genetically identical clone, that meant that mutations built up quite early in the course of experimental evolution. That variation corresponded to differences in the fitness of strains within the population—and the success or failure of the loss-of-sex mutation depended on whether it turned up in a strain that was already pretty fit to begin with.

Without recombination to mix up the genome, a beneficial mutation is bound to genetic variants at many, many other loci that may boost the benefits from that mutation, or cancel them out. In a clonal population, each genome succeeds or fails as a unit—a single useful mutation simply cannot do it alone.

References

Lang, G., Botstein, D., & Desai, M. (2011). Genetic variation and the fate of beneficial mutations in asexual populations. Genetics DOI: 10.1534/genetics.111.128942

Lang, G., Murray, A., & Botstein, D. (2009). The cost of gene expression underlies a fitness trade-off in yeast. Proc. Nat. Acad. Sciences USA, 106 (14), 5755-60 DOI: 10.1073/pnas.0901620106

Released from predators, guppies reshape themselves—and their environment

A (domestic) male guppy. Photo by gartenfreuden.

ResearchBlogging.orgConsider a population of guppies living in the Aripo River in Trinidad. They have a happy existence, as far as guppies can be happy, but their lives are shaped by the constant threat of larger, predatory fish. The river runs clear over a colorful gravel bed, and guppies who stand out against that background are eaten quickly. Even guppies whose coloration helps them blend in have to be ready to make a break for it if a predator shows up. All in all, a guppy’s chances of surviving to mate depends most on its ability to hide from bigger fish, and to swim quickly when it can’t hide.

Then one fine day a biologist comes along, scoops up a couple hundred guppies, and moves them to a pool in a tributary of the river. The pool is separated from the mainstream by a series of waterfalls, so larger fish can’t swim up—the guppies are now free from their most dangerous predators. They can be fruitful and multiply. In this new habitat, camouflage and evasive maneuvers don’t matter so much. What does matter is finding enough food to make some babies in the midst of a whole bunch of other guppies who are also not particularly worried about predators.

John Endler started the experiment I’ve just described back in 1976 to see whether guppies’ coloration helps them hide from predators [PDF]. The guppies he moved to a predator-free stream have continued to evolve, though, and three decades later, new studies are showing how release from predators changed the guppies—and how those changed guppies could be changing the living community around them.

Since the 1976 introduction, Endler and other biologists have tracked the Aripo River guppies’ response to the change in natural selection he created. Release from predators is considered one of the classic sources of ecological opportunity that can free a population to evolve new traits and behaviors, and explore new ways of making a living. At the same time, a sudden lack of predators means that competition within the population can become stronger.

Points of measurement for guppy body and head shape, illustrated on a stained specimen. Image from Palkovacs et al, fig. 1.

In one study just published by PLoS ONE, Eric Palkovacs and two colleagues compared the body shape of guppies from the experimental population with guppies from the source stream. (Endler had noted changes in body shape along with changes in coloration in his original paper.) First, Palkovacs and his coauthors gauged how rapidly female guppies taken from each site snapped up standardized food. Then they killed the test fish, treated them with stain, and measured their body and head shape. Fish from the site with lower predation ate faster, and they had bigger mouths and deeper bodies than fish from the site with more predators.

Palkovacs and his coauthors also observed that the guppy populations at the experimental site were denser—without predators thinning them out, the fish are probably most limited by their food supply. A study published last year in PNAS suggests that this denser guppy population might reshape its own environment. The paper’s authors created artificial ponds stocked with algae and small invertebrates, then introduced guppies from the high-predation source site or from the low-predation experimental site. They also controlled for the differences in guppy population density associated with predator pressure, maintaining the fish at either the high density observed with low predation, or the lower density observed with high predation.

Where the guppies came from made a significant difference in the artificial ecosystems, and these differences were in some cases exaggerated by the increased population density caused by predator release. Guppies from the “released” site ate less selectively than guppies from the site experiencing higher predation, who favored invertebrates over algae. As a result, guppies from the released site were associated with less algae growth, and higher invertebrate population density. Probably because they ate more plant matter, guppies from the released site also excreted less nitrogen, reducing the nutrient’s availability for plant growth.

These results echo a study I discussed last year, which used a very similar approach to show that speciating sticklebacks can change their environment. It’s another reminder that evolutionary change can feed back to change the environmental conditions that prompted change in the first place—that natural selection operates in the midst of continuous change.

References

Bassar, R., Marshall, M., Lopez-Sepulcre, A., Zandona, E., Auer, S., Travis, J., Pringle, C., Flecker, A., Thomas, S., Fraser, D., & Reznick, D. (2010). Local adaptation in Trinidadian guppies alters ecosystem processes. Proc. Nat. Acad. Sciences USA, 107 (8), 3616-21 DOI: 10.1073/pnas.0908023107

Endler, J. (1980). Natural selection on color patterns in Poecilia reticulata. Evolution, 34 (1), 76-91 DOI: 10.2307/2408316

Palkovacs, E., Wasserman, B., & Kinnison, M. (2011). Eco-evolutionary trophic dynamics: Loss of top predators drives trophic evolution and ecology of prey. PLoS ONE, 6 (4) DOI: 10.1371/journal.pone.0018879

Deprived of pollinators, flowers evolve to do without

Who needs pollinators? Not monkeyflowers—at least not after a few generations of evolution. Photo by Brewbooks.

ResearchBlogging.orgThe loss of animal pollinators poses a potentially big problem for plants. However, many plant species that rely on animals to move pollen from anther to stigma have the capacity to make due if that service goes undone—and, as a new study released online early by the journal Evolution demonstrates, such plants can rapidly evolve to do without pollinators [$a] if they must.

The paper’s authors, Sarah Bodbyl Roels and John Kelly, demonstrate this using a simple greenhouse experiment with the monkeyflower Mimulus guttatus, a wildflower native to western North America, and a member of a genus rapidly developing into a major model system for studying the evolution of ecological isolation and floral evolution.

Mimulus species vary in their reliance on animal pollinators—some grow minimalistic flowers, with the anther so close to the stigma that pollen transfers without any assistance. In natural populations, M. guttatus is usually pollinated by bees, but individual plants vary in the distance between anther and stigma, and this variation has a genetic basis. So a population of M. guttatus deprived of pollinators would have the raw material to evolve a solution—natural selection would favor plants that are better able to self-pollinate. As the population evolved to be more self-fertilizing, it might also evolve to look more like self-pollinating Mimulus species, losing the bright petals that attract pollinators.

To see whether this could actually happen, Bobdyl Roels and Kelly challenged an experimental population of Mimulus guttatus to do without pollinators, and tracked its response.

The authors raised seeds derived from a natural wild population of Mimulus guttatus in greenhouses under two trial conditions: control populations were provided with hives of bumblebees to pollinate them when their flowers were ready for servicing; and experimental populations were left to produce what seed they could without pollinators. The authors collected the seeds produced by each population, and planted them to form the next generation.

A bumblebee digs for nectar in flowers of Mimulus moschatus. Photo by Mollivan Jon.

Early on in the experiment, the experimental populations deprived of pollinators fared badly. Without pollinators, the average plant produced two seeds or fewer by the end of the generation, compared to eight or ten seeds per plant in the population provided with bees. By the fifth generation, however, this was starting to improve—plants in both populations without pollinators were producing more seeds, and one of the two experimental populations produced nearly as many seeds as the control plants.

Examining the traits of plants produced by this final generation (actually, the grand-offspring of the fifth generation, to control for effects of inbreeding), the authors found that the average distance between the pollen-producing anther and the pollen-receiving stigma had shrunk significantly in plants from the experimental population. Across all the treatments, plants with a shorter distance between stigma and anther produced more self-pollinated seeds. There was no evolved change in other floral measurements, however—plants in the no-pollinators treatment had petals as big and showy as plants evolved with bumble bees.

In a natural population of Mimulus guttatus, the drop-off in seed production created by loss of pollinators should have much the same effect as in this experiment, creating a strong selective advantage for individual plants that can make more seeds on their own. The fact that the experimental plants did not evolve reduced petals could mean that in the cushy conditions of a greenhouse, there wasn’t much need to stop spending resources making showy flowers. Or maybe, when the major source of natural selection is the need to make any seeds at all, selection to save resources on flower production is relatively weak and correspondingly slow-acting.

As the authors point out, one of many changes humans are making to natural communities around the world is to disrupt pollination relationships. In a sense, experiments like theirs are being carried out worldwide, on hundreds of plant species—and each species will adapt, or fail to adapt, in its own way.

Reference

Bodbyl Roels, S., & Kelly, J. (2011). Rapid evolution caused by pollinator loss in Mimulus guttatus. Evolution DOI: 10.1111/j.1558-5646.2011.01326.x

What’s in that dissertation, anyway?

About to take the plunge. Photo by jby.

So, what with getting my sparrows in a row for my dissertation defense on Friday, I haven’t written any new science post for this week. But! As it happens, I have written about most of the component chapters of my dissertation—so in lieu of something new this week, why not check out those posts?

  • The first chapter of my dissertation is a literature review about the phenomenon ecologists call ecological opportunity, and how it may or may not explain big, rapid evolutionary changes. I’ve also written about this topic for the Scientific American guest blog.
  • The second chapter uses phylogenetic methods to reconstruct what yucca moths were like before they were yucca moths.
  • The third chapter presents a mathematical model of coevolution between two species, and determines what kind of interactions—predation, parasitism, mutualism, competition—can cause those species to evolve greater diversity.
  • The fourth chapter is the latest work on my lab’s big study of Joshua trees and their pollinators. The material I’m including in this chapter hasn’t been reviewed and published yet, but you can read the most recent Joshua tree post to learn what we know so far, and what kinds of questions we still want to answer.

Regular posting resumes next week, provided that I pass my defense and the celebrating afterward doesn’t interfere with my blogging capacity.