The living rainbow: The selective benefit of a fa’afafine in the family

ResearchBlogging.orgOne of the key evolutionary puzzles of same-sex sexuality, as it manifests in modern, Western human societies, is that those of us attracted to members of our own biological sex don’t make a lot of babies. I’ve already spent a lot of pixels on the question of how genes for same-sex attraction might persist in human populations in the face of that selective cost—but a paper just published in PLoS ONE adds some evidence in favor of one popular hypothesis: that gene variants that make men more likely to be gay could also make their straight relatives more fertile.

The new paper presents data from Samoa, where the traditional culture has long had a place for men who are attracted to other men, in the role of fa’afafine—literally, men who “live in the manner of women.” Samoan boys who show interest in feminine activities are recognized by their families as members of this “third gender,” which is more like the modern Western conception of transgender identity than what we call “gay.” Fa’afafine often present and dress like straight women, and as adults, they generally have relationships with straight-identified men. But fa’afafine aren’t exactly “transgendered” as we understand that concept in the West—they don’t have the sense that their bodies don’t match their gender identity.

The fact that Samoan culture accommodates and accepts same-sex sexuality makes it an especially interesting context for testing hypotheses about the evolution of queer sexuality, including the idea that relatives of fa’afafine might be more fertile than people with no fa’afafine in the family. The study’s coauthors surveyed Samoan fa’afafine and straight men, asking how many children their grandmothers, aunts, and uncles had had. And they found that grandmothers of fa’afafine—both maternal and paternal grandmothers—had more children than grandmothers of the straight-identified men they interviewed.◼


VanderLaan, D., Forrester, D., Petterson, L., & Vasey, P. (2012). Offspring production among the extended relatives of Samoan men and fa’afafine. PLoS ONE, 7 (4) DOI: 10.1371/journal.pone.0036088

Notes from the field: What’s Chris doing to that Joshua tree?

Joshua tree, diverged. Photo by jby.

Cross-posted from Nothing in Biology Makes Sense!

ResearchBlogging.orgMy postdoctoral research is shaping up more and more to be hardcore bioinformatics; apart from some time spent trying to get a dozen species of peanut plants to grow in the greenhouse as part of a somewhat long-shot project I’m working on with an undergraduate research associate, I mostly spend my workday staring at my laptop, writing code. It’s work I enjoy, but it doesn’t often give me an excuse to interact directly with the study organism, much less get outdoors. So, when Chris Smith dropped the hint that he could use an extra pair of hands for fieldwork in the Nevada desert this spring, I didn’t need a lot of persuasion.

Chris is continuing a program of research he started back when he was a postdoc at the University of Idaho, and which I contributed to as part of my doctoral dissertation work. The central question of that research is, can interactions between two species help to create new biological diversity? And the specific species we’ve been looking at all these years are Joshua trees and the moths that pollinate them.

Joshua trees, the spiky icon of the Mojave desert, are exclusively pollinated by yucca moths, which lay their eggs in Joshua tree flowers, and whose larvae eat developing Joshua tree seeds. It’s a very simple, interdependent interaction—the trees only reproduce with the assistance of the moths, and the moths can’t raise larvae without Joshua tree flowers. So it’s particularly interesting that there are two species of these highly specialized moths, and they are found on Joshua trees that look … different. Some Joshua trees are tall and tree-ish, and some Joshua trees are shorter and bushy. Maybe more importantly for the moths, their flowers look different, too.

Joshua trees, diverged. Photo by jby.

Here’s a photo of two of those different-looking Joshua tree types, side by side in Tikaboo Valley, Nevada. Tikaboo Valley has the distinction of being the one spot where we’ve found both of the tree types, and both of the pollinator moth species, living side by side. That makes Tikaboo Valley the perfect (well, only) place to figure out whether there’s an evolutionary consequence to the divergence of Joshua tree and its association with two different pollinators. Do Joshua trees make more fruit, or fruit with more surviving seeds, when they’re pollinated their “native” moths?

So, over several years of work at Tikaboo Valley, we’ve been edging towards answering that question. We’ve found evidence that, given access to both tree types, the two moth species spend more time on their “native” tree type, and have more surviving offspring when they lay eggs in “native” flowers. But to determine whether plant-pollinator matching matters to Joshua trees, we’d really like to find out what happens when each moth species is forced to use each type of tree, and that’s what Chris has been working on for the last several field seasons.

Installing a Joshua tree chastity device. Photo by jby.

The method for the experiment, developed after some false starts, goes like this:

  • Find Joshua trees with flowers that haven’t opened yet—untouched by pollinating moths;
  • Make sure said flowers are far enough off the ground to be out of reach of the open-range cattle that graze all over Tikaboo Valley;
  • Catalog the tree, measuring how tall it grew before it started branching (a good indicator of which type of tree it is), and its total height, and take a nice photo of it with an ID number placed nearby, for handy future reference;
  • Seal up the not-yet-open bunch of flowers inside fine-mesh netting, to keep moths out—and also, as we’ll see below, to keep moths in;
  • Cover the netted flowers in chicken wire, to keep out all the desert critters that like to eat Joshua tree flowers, even if said flowers are served with a side of netting;
  • While the flowers get closer to opening, go collect some yucca moths, which you do by cutting down clusters of open Joshua tree flowers, dumping them into a bag or a cloth butterfly net, and sorting through the flowers looking for fleeing moths, which can be guided into plastic sample vials—these moths don’t usually like to fly; and finally
  • Open caged flowers, and insert moths.

By introducing moths of each species into flowers on each variety of Joshua tree, we’ll be able to see whether trees with the “wrong” moth species are less likely to make fruit than trees with the “right” moth species; and directly verify that moths introduced into the “wrong” tree type have fewer surviving larvae than moths introduced into the “right” tree type.

Camp Tikaboo, 2012 edition. Photo by jby.

But, being desert plants, Joshua trees aren’t prone to making much fruit even under ideal conditions. After a dry winter (like this last one), it can be hard to find any flowering trees at all. So to obtain a respectable sample size takes a lot of folks—this year, I was one of ten people on the field crew camped in the middle of the valley: a cluster of tents grouped around a rented recreational vehicle, which served as a kitchen/gathering area/lab.

Chris’s lab tech, Ramona Flatz, kept the whole show organized, dividing us into teams to scout for trees with flowers, teams to follow up on scouting reports and install experimental net/cage setups, and teams to go collect moths to put in the cages. This planning was, naturally, conducted in a tent containing a table with laminated maps of the valley, and this tent was called, naturally, the “war tent.”

In the “war tent,” making plans. Photo by jby.

What results we’ll get remain to be seen; this is the second year with a substantial number of experimental trees, and we won’t know whether all that work has borne fruit until Chris returns in a few weeks to see whether any of the experimental trees have, er, borne fruit. As far as I’m concerned, it was wonderful to return to an old familiar field site, in the middle of the desert, and spend a few days hiking around and harassing yucca moths instead of anwering e-mail. But if the experiment works, the results should be mighty interesting.

Below, I’ve embedded a slideshow of all the photos I took over a few days at Tikaboo Valley—including a special moth-themed production number coordinated by Ramona.◼


Godsoe, W., Yoder, J., Smith, C., & Pellmyr, O. (2008). Coevolution and divergence in the Joshua tree/yucca moth pollination mutualism The American Naturalist, 171 (6), 816-823 DOI: 10.1086/587757

Smith, C. I., C. S. Drummond, W. K. W. Godsoe, J. B. Yoder, & O. Pellmyr (2009). Host specificity and reproductive success of yucca moths (Tegeticula spp. Lepidoptera: Prodoxidae) mirror patterns of gene flow between host plant varieties of the Joshua tree (Yucca brevifolia: Agavaceae) Molecular Ecology, 18 (24), 5218-5229 DOI: 10.1111/j.1365-294X.2009.04428.x

Yoder, J., & Nuismer, S. (2010). When does coevolution promote diversification? The American Naturalist, 176 (6), 802-817 DOI: 10.1086/657048

Do choosy cuckoos choose well-matched hosts?

A reed warbler feeds a cuckoo chick. Photo via Wikimedia Commons.

ResearchBlogging.orgCross-posted from Nothing in Biology Makes Sense.

Brood parasitism, the reproductive strategy of choice for cuckoos and cowbirds, sounds like a lazy approach to parenting: lay your eggs in another bird’s nest, and let the unwilling adoptive parents take the trouble to raise your chicks. But contracting out parental care like this comes with many of its own complications. Chicks raised by parents of a different species have to eliminate competition from their adoptive nestmates, and may grow up a bit confused; reluctant host birds may need to be told, and reminded, that raising cuckoo chicks is an offer they can’t refuse.

But before crossing all those hurdles, a brood parasite’s first task is to lay eggs in the nest of a host who won’t immediately recognize and reject them. The strong natural selection imposed by host rejection has led cuckoos to evolve “host races” that lay eggs whose color and spotting pattern matched to those of their preferred host species. This kind of broad-scale pattern could arise without much direct effort by female cuckoos—those who lay eggs in the nest of the best matching host species would simply be the ones most likely to have chicks that survive to the next generation. But is it possible that cuckoos do take an active role in matching up to their hosts, seeking out host nests containing eggs that look like their own?

The answer, according to a series of studies over the last several years, is yes—probably.

Cuckoo eggs (indicated by arrows) in the nests of three different host species. Illustration via The Knowledge Project.

Although the match between cuckoos’ eggs and those of the specific host species whose nests they invade is striking even to human eyes, it had been generally assumed that, within these egg-matching associations, cuckoos could choose nests pretty much at random. That is to say, while the differences in coloration and spotting between the eggs of different host species were enough to make it hard for a cuckoo egg to blend in with the nests of redstarts and warblers at the same time, a cuckoo whose eggs match the eggs of one redstart will also match the eggs of most other redstarts.

A 2006 study suggested this thinking might be wrong. A group of European ornithologists took advantage of a handy “natural experiment” on the Dutch island of Zealand, where cuckoos had been absent until the early twentieth century. Using museum specimens of cuckoo eggs and eggs from the reed warbler nests in which they were collected, the team compared the match between cuckoo egg color and host egg color over time. Improved matching could be due to female cuckoos selecting better-matched host nests in the new host population; but it could also be created by simple natural selection—the colonizing cuckoos evolving eggs that better matched the host population on average. The coauthors found evidence of rapidly improved matching—but no evidence that the cuckoo’s egg color had changed overall. It looked like the newly arrived brood parasites were adapting by learning, or by evolving, preference for better matches.

Some of the same ornithologists followed this result with a small 2007 study that more directly examined the role of host choice by cuckoos. At a field site in Hungary, they measured the match between cuckoo eggs laid in the nests of great reed warblers, and compared the rate at which warbler parents ejected the naturally-laid cuckoo eggs to the rate at which they rejected randomly-drawn cuckoo eggs introduced into their nests by members of the research team. They found that, indeed, the cuckoo-laid cuckoo eggs were better matches to the eggs in their host nests than researcher-laid cuckoo eggs were—and, more importantly, warblers were less likely to reject the better-matched cuckoo-laid eggs.

A great reed warbler is probably ready for this cuckoo chick to leave the nest. Photo by phenolog.

This result was somewhat complicated, however, by a study just published in PLoS ONE. This time the authors, again including many of the same ornithologists involved in the original 2006 study, compared the match between cuckoo eggs laid in marsh warbler nests at a site in Bulgaria to the cuckoo eggs’ potential match with warbler eggs in nearby unparasitized nests.

If cuckoos were choosing the best-matched host nests, the authors reasoned, there should be a better match between cuckoo eggs and the eggs in parasitized nests than in nearby nests, which the same cuckoo could have used, but didn’t. Six years after the original cuckoo choosiness study, the team was able to use a new approach to compare the match between host and cuckoo eggs: rather than simply compare the spectrum of light reflected by the eggs, they fed the measured spectrum into a mathematical model of bird vision—an approach used in other studies of brood parasites, which is thought to be superior because it estimates how similar, or different, two eggs look through the eyes of a host parent.

With this approach, the team found that cuckoo eggs were not siginificantly better matched to warbler eggs in parasitized nests than they were to eggs in nearby unparasitized nests. Did this overturn the previous evidence for choosy parasitic parents? Well, maybe.

On the one hand, the new study uses the new vision model comparison method, which should give more biologically meaningful results. But on the other, the new study’s design is different in from the 2007 study in a critical way: it doesn’t tell us whether cuckoos’ host choices make the hosts less likely to reject cuckoo eggs. In the 2007 study, there was no need to guess whether the statistical comparison of egg color spectra was biologically meaningful—host parents “told” the researchers that the comparison mattered by rejecting randomly-chosen cuckoo eggs more often than they did eggs laid by actual cuckoos.

So, although there are good reasons to think that the form of measurement used in the new study is better, it’s not clear to me that the result is actually more useful for understanding how natural selection could be acting on cuckoos choosing among many available host nests in a single population. What I’d like to see is a study using the field methods of the 2006 study, and the color matching methods of the 2012 one. ◼


Antonov, A., Stokke, B., Fossøy, F., Ranke, P., Liang, W., Yang, C., Moksnes, A., Shykoff, J., & Røskaft, E. (2012). Are cuckoos maximizing egg mimicry by selecting host individuals with better matching egg phenotypes? PLoS ONE, 7 (2) DOI: 10.1371/journal.pone.0031704

Avilés, J., Stokke, B., Moksnes, A., Røskaft, E., Åsmul, M., & Møller, A. (2006). Rapid increase in cuckoo egg matching in a recently parasitized reed warbler population Journal of Evolutionary Biology, 19 (6), 1901-10 DOI: 10.1111/j.1420-9101.2006.01166.x

Cherry, M., Bennett, A., & Moskat, C. (2007). Do cuckoos choose nests of great reed warblers on the basis of host egg appearance? Journal of Evolutionary Biology, 20 (3), 1218-22 DOI: 10.1111/j.1420-9101.2007.01308.x

In flour beetles, coevolution mixes things up

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. ◼


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

Color indicates poison in “poison dart” frogs—honestly!

A strawberry poison dart frog; apparently the San Cristobal color morph. Photo by Wilfredo Falcón.

ResearchBlogging.orgAlmost everyone knows the basic story behind the brilliant coloring of poison dart frogs. These tiny tropical rainforest amphibians secrete toxic alkaloids from their skin, and their bright colors are aposematic signals to warn away potential predators.

You’d expect species that are all sending the same message—Poison! Don’t eat!—to use the same signal to do it. Local studies confirm that birds are more likely to attack poison dart frogs who look different from other poison dart frogs in a given area. Yet not all poison dart frogs have the same color pattern, or even similar color patterns. Far from it—frogs within the same species can look completely different.

One possible explanation is that frogs with different coloration are not, in fact, sending the same signal. Brighter color could indicate greater toxicity. That seems to be the case for one highly variable species, the strawberry poison dart frog Dendrobates pumilio. A paper just published as an online, open-access article in The American Naturalist demonstrates that D. pumilio‘s colors are “honest signals”—and those signals are directed at specific predators.

The many colors of Dendrobates pumilio. Figure 1 from Maan & Cummings (2012).

The new study’s authors, Martine Maan and Molly Cummings, selected a study species that is a veritable rainbow of aposemitism, as you can see from the excerpted figure above. Different populations of Dendrobates pumilio are orange, red, green, blue, and yellow, with or without black spots. Maan and Cummings make sense of that colorful diversity in two major ways: first, by finding out whether there’s a relationship between color and poison, and second, by making an educated guess about how the different color morphs look to D. pumilio‘s many predators.

For the first part, Maan and Cummings took an objective measure of color—reflectance spectrum of frogs’ skin, measured under standardized lighting—and compared it to an objective measure of toxicity—how much discomfort mice exhibited from an injection of frog skin extract. (The mouse injection method is apparently a standard toxicity assay, and I guess it makes sense if you don’t know the specific chemicals that make the frogs poisonous.) The coauthors found a strong relationship between skin brightness and toxicity—frogs with brighter coloring were more poisonous.

Objectively bright coloring isn’t quite the same thing as looking bright to a predator, though. Different animals have different color vision—a frog that looks brightly colored to a frog-eating bird might not be particularly showy to a frog-eating snake, because birds and snakes have different suites of sensory cells in their eyes. So the coauthors then fed the spectral readings from the frogs into mathematical models that estimate how the frogs look to different kinds of animal vision. (This approach has been used elsewhere—for instance, to determine how well brood-parasitic cuckoo eggs blend in with their hosts’.) Maan and Cummings applied models based on the visual sensitivity of crabs, snakes, two kinds of bird vision, and frog vision.

Another strawberry poison dart frog, this time the color morph found on Aguacate. Photo by Drriss.

They found strong relationships between the frogs’ toxicity and their colors as seen by birds, and as seen by other frogs. The crab vision model varied depending on what kind of material the frog would be viewed against—to a crab, the frogs were conspicuous against bark or leaf litter, but not against green leaves. Meanwhile, the snake vision model didn’t perceive any particular relationship between brightness and toxicity. Those results make a lot of sense. Birds are most likely to spot prey from a distance, and make a decision to pursue it or not without getting up close. Crabs aren’t likely to encounter frogs up in the foliage, but on the ground, in the leaf litter. And snakes are less likely to rely sight than on chemical senses—taste or olfaction—in evaluating a potential meal.

This study doesn’t directly demonstrate the action of natural selection, and that leaves a significant question hanging: Why should Dendrobates pumilio signal its toxicity honestly? Certainly, if you’re a highly toxic frog, you’d want to let predators know; but if you’re less toxic than the frogs in the next population, why would you tell the world? Indeed, other species of poison dart frogs have evolved mimicry—bright colors without poison.

That suggests the honest coloration within D. pumilio is be due to more than just selection by predators. Perhaps coloration serves social functions, and then more conspicuous color morphs need to be more toxic to fend off more frequent predator attacks. Or there may be genetic constraints that link bright color and toxicity within the species, and both have evolved local differences due to genetic drift. Finding out how selection and other evolutionary forces have created this pattern would be no small project, but I think it’ll make an interesting story in the end. ◼


Darst, C. (2006). A mechanism for diversity in warning signals: Conspicuousness versus toxicity in poison frogs Proc. Nat. Acad. Sciences USA, 103 (15), 5852-7 DOI: 10.1073/pnas.0600625103

Maan, M., & Cummings, M. (2012). Poison frog colors are honest signals of toxicity, particularly for bird predators. The American Naturalist, 179 (1) DOI: 10.1086/663197

Frightened birds make bad parents

Song sparrow chicks. Photo by Tobyotter.

ResearchBlogging.orgPredators have an obvious impact on their prey: eating them. But if the threat of predators prompts prey species to change their behavior, those behavioral changes can also affect prey population dynamics [$a]—and thereby, potentially, the prey’s evolution—even if the predators never actually catch any prey.

This is the effect documented in a short, sharp study just published in Science, in which Liana Y. Zanette and her coauthors show that song sparrows raise fewer chicks if they simply think that there are predators nearby [$a].

The team’s experimental design was simple but probably pretty work-intensive. Over the course of one summer on several small islands off the coast of British Columbia, they watched song sparrows choose mates and build nests. Once nests were established, the team surrounded them with anti-predator defenses: netting and electrified fences. They confirmed that these measures kept predators out with regular video surveillance. And then they turned on the loudspeakers.

At some nests, the team broadcast looped recordings of calls made by song sparrow predators—raccoons, crows and ravens, hawks, owls, and cowbirds. At control nests, the broadcast was instead a playlist of similar-sounding calls made by non-predators, including seals, geese, hummingbirds, and loons. The team then monitored the nests, recording the behavior of the mated pair at each nest, and the ultimate success of the eggs they laid.

An adult song sparrow, looking watchful. Photo by kenschneiderusa.

The results are pretty unambiguous. Pairs of song sparrows that heard predator calls laid fewer eggs than pairs that heard non-predators. Of the eggs laid by pairs who heard predator calls, fewer hatched, and of those hatched chicks, fewer survived fledge. Just the continuous, threat of predators—predators that were never visible—reduced the number of chicks the sparrows fledged.

The reasons for the reduced offspring are apparent from other behavioral observations. Birds in the predator-call treatment were perpetually on high alert, as measured by “flight initiation distance,” the distance up to which a researcher could approach the nest before the birds took flight. Sparrows in the non-predator treatment let researchers get about 120 meters from the nest before taking off; sparrows in the predator treatment wouldn’t tolerate humans within twice that distance. In the predator treatment, sparrows spent less time sitting on their eggs, and visited to feed their chicks less frequently. Not surprisingly, chicks in the predator treatment also gained less weight than chicks in the non-predator treatment.

And, in what may be the most poignant data set I’ve ever seen in print, the team also measured the skin temperature of chicks in each nest 10 minutes after the parents had left. Chicks in the predator-call treatment were measurably, and significantly, colder.

So the simple fear of predators is enough to prompt free-living song sparrows to lay fewer eggs, and raise fewer of the eggs they do lay to fledging. However, the absolute difference in offspring between sparrow pairs in the predator and non-predator treatments—40%—probably reflects the maximum effect we might expect to see in natural populations.

That’s because left to themselves, sparrows probably seek nesting spots with less predator activity. Here, all the sparrows had established nests in what, presumably, were the best spots they could find—but for half of them, the new neighborhood suddenly seemed to become a lot less safe shortly after they settled in. What Zanette et al. document is very much a behavioral, short-term response, and it’s one that many prey animals may be able to mitigate, or avoid altogether, with other behavioral responses. It’s hard to say how exactly it reflects the impact that fear of predators might have in sparrow populations unmolested by ornithologists.

Nevertheless, this result does suggest that for many prey animals, the fear of predators can, itself, be something to fear. ◼


Creel, S., & Christianson, D. (2008). Relationships between direct predation and risk effects. Trends in Ecology & Evolution, 23 (4), 194-201 DOI: 10.1016/j.tree.2007.12.004

Martin, T. (2011). The cost of fear. Science, 334 (6061), 1353-4 DOI: 10.1126/science.1216109

Zanette, L., White, A., Allen, M., & Clinchy, M. (2011). Perceived predation risk reduces the number of offspring songbirds produce per year. Science, 334 (6061), 1398-1401 DOI: 10.1126/science.1210908

Can’t keep us apart: Brood parasitic birds have specialized on the same hosts for millions of years

A male greater honeyguide. Photo via Safari Ecology.

ResearchBlogging.orgBrood parasitic birds lay their eggs in other birds’ nests, a lazy approach to parenting that shapes the behavior and evolution of brood parasites in all sorts of interesting ways.

Brood parasite chicks often kill their adoptive nestmates, and can grow up confused about their species identity. To better trick their hosts into accepting “donated” eggs, many brood parasites have evolved eggs that mimic the hosts’—and some hosts have evolved contrasting eggs in response. A recent genetic study now shows an even subtler pattern arising from this host-parasite coevolutionary chase: lines of parasitic females that have specialized on the same host species for millions of years.

The brood parasite in question is the greater honeyguide, an African bird best known for helping people find bee colonies (though the story that honeyguides also guide honey badgers don’t have much factual basis). However, honeyguide females also lay their eggs in the nests of several host species—including hoopoes, greater scimitarbills, green woodhoopoes, little bee-eaters, and striped kingfishers. Although the honeyguides’ eggs aren’t colored like their hosts’, they do have matching shapes—the hosts all nest in tree cavities, where lighting is too poor to notice a mis-colored egg, but an oversized or oddly shaped one would stand out.

A hoopoe, one of the birds that “adopts” greater honeyguide eggs. Photo by Hiyashi Haka.

There’s an evolutionary catch, though: hoopoes, scimitarbills, and woodhoopoes lay oblong eggs, while the bee-eaters and kingfishers lay spherical eggs. Yet honeyguide females manage to lay eggs of matching shape and size in the nest of each host. Individual brood parasites can’t adjust the shapes of their eggs to match those in a host nest—they find hosts with eggs that will match their own.

How do they do it? Maybe each female honeyguide actually goes looking for nests like the one she grew up in, either because she is compelled to by some genetic instinct, or because she learns to recognize a potential host in the course of being raised by that host. Or maybe the host birds are so good at recognizing and rejecting oddly-shaped parasite eggs that only well-matched eggs make it to adulthood. Any of these processes could result in long lineages of female honeyguides laying eggs in the nests of the same host species their mothers, grandmothers, and great-grandmothers used. This is precisely the pattern Claire Spottiswoode and her coauthors found in the population genetics of greater honeyguides.

Spottiswoode et al. collected genetic data from honeyguides using all five of the host species mentioned above, and compared the patterns of relatedness from different genetic markers to patterns of host use. The pattern of differentiation in a marker from the mitochondrial genome—genes contained in the mitochondria, which mothers pass on to their offspring but fathers do not—neatly divides the honeyguides between hosts with oblong eggs and the hosts with spherical eggs. By applying a molecular clock to the mitochondrial data, the team found that the division between oblong-egg and spherical-egg honeyguides dates back as long as 3 million years ago. So honeyguide females have been tracking the same hosts, or very similar ones, for quite some time!

However, no such pattern is evident in four genetic markers from the nuclear genome, which is inherited via both parents. That suggests male honeyguides don’t discriminate among females based on host fidelity—mates pair off regardless of what host species they each grew up with. Spottiswoode et al. also note that this result hints at how honeyguide egg characteristics and host preferences could be inherited: via the female sex chromosome. In birds, biological sex is determined by the Z and W chromosomes—individuals with two Z chromosomes develop as males, and individuals with a Z and a W chromosome develop as females. Host preferences and egg shape inherited via the W chromosome would then be carried only by females.

However, the data presented here don’t directly test the W-chromosome hypothesis. That would require markers—or better yet complete sequence data—from the W chromosome itself, and (to be really thorough) lots more markers from the rest of the nuclear genome as well. That’s a lot of genetic data to collect, but we are very close to the day when such data are easily collectible. ◼


Spottiswoode, C., Stryjewski, K., Quader, S., Colebrook-Robjent, J., & Sorenson, M. (2011). Ancient host specificity within a single species of brood parasitic bird. Proc. Nat. Acad. Sciences USA, 108 (43), 17738-42 DOI: 10.1073/pnas.1109630108

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

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. ◼


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

What does evolution have to do with the cost of police in Switzerland? Probably not much.

Lucerne, Switzerland. Photo by Jamie McHale.

ResearchBlogging.orgSo a little while ago, I was perusing the latest from PLoS ONE while doing some low-attention-requiring lab work Monday afternoon, and a title caught my eye: “A test of evolutionary policing theory with data from human societies.” Oh, hey. That looked interesting.

The paper’s author, Rolf Kümmerli, claims to have found evidence for a particular kind of evolutionary model of cooperation in recent economic data from Switzerland. The problem Kümmerli addresses is a classic one: from the perspective of natural selection, individuals (apparently) have little evolutionary incentive to cooperate, unless they’re relatives. And yet, we see cooperation in human societies.

One solution to this quandary has been group-level selection, which is a whole ‘nother kettle of worms. Another is that policing behavior could evolve to help keep groups of less-closely-related people cooperative. Of course, modern human societies are a long way past the days when most of us lived in villages that were also basically big extended families. Kümmerli proposes that we might use some sort of rule of behavioral thumb to (unconsciously) assess how likely it is we’re interacting with close relatives—which is less likely in bigger communities, and communities with larger immigrant populations.

Er, what?

Kümmerli compiled data from the Swiss national government, comparing crime rates and police expenditures to the population size percentage of foreign nationals living in every Swiss canton, or administrative region. Rather than just use the raw population size or percentage of foreigners in each canton, he constructed an index that combines the two. And he did, indeed, find that as this index of “dissimilarity” increases, so do crime rates and expenditures on police.

Kümmerli concludes that his data support the “evolutionary policing theory.” But what has he actually shown? Crime happens for lots of reasons, not necessarily because people somehow “know” to behave more cooperatively in small towns. Most glaringly, Kümmerli’s data set includes no data on poverty, which seem like an obvious alternative explanation for the pattern—bigger communities with more immigrants also often have more poor people, and poverty is certainly related to crime rates.

Swiss police. Photo by Kecko.

Fortunately, the data Kümmerli uses, and many more variables, are all freely available online through the Swiss Statistical Encyclopedia. So I took a couple hours to play around with the raw numbers. I did all my statistical work in good old R.

For each of the 26 cantons, I compiled the number of reported crimes in 2009, the number of citizens (in thousands) in 2009, the percentage of foreign residents in 2009, the percentage of unemployed residents in 2010, annual expenditures on police in 2008, and—just for the heck of it—the percentage of commuters using public transit in 2000. As in Kümmerli’s data set, each statistic is the most recent value available. I didn’t try to replicate Kümmerli’s “dissimilarity” index because it’s not clearly explained in the paper; but I did log-transform the crime rate, the number of citizens, police expenditures, the unemployment rate, and the transit use rate to make them better conform to a normal distribution.

Here’s what the simple linear relationships among all those variables look like. Apologies for the complicated graphic, but this is a complex data set.

Linear relationships (upper triangle) and correlation coefficients (lower triangle) among variables from the Swiss Statistical Encyclopedia. Grapic by jby.

In the upper triangle of this matrix, you can see scatter plots with linear regression lines estimated from the data. Regression lines are colored according to statistical significance, corrected for multiple testing: red lines are “very” significant, orange just significant; grey lines indicate relationships no stronger than expected by chance. The bottom triangle gives the raw correlation coefficient between the variables, on a scale where 1 means a perfect relationship and 0 means no relationship.

What you should notice first is that top row of scatterplots, which show that crime rates have strong linear relationships with every other variable in the dataset, from population size to mass transit use. But that makes a certain amount of sense—all these variables are interrelated. Larger communities tend to attract more immigrants and tend to have better public transit systems that support more use. Communities with more unemployed people might have higher mass transit use, since cars are expensive. So, lots of correlation—but is there any causation in there?

There are a number of ways to tackle that question. A relatively easy one is to use multiple regression and a “model comparison” approach. This essentially builds a statistical model in which multiple variables—population, foreign residents, unemployment, mass transit use—are used to predict a single variable, crime rates. The procedure then compares the model’s AIC score, an index of the model’s ability to predict crime rates from the other variables, to models with each of the individual variables removed. If removing a variable makes a “significant” reduction in AIC—which is typically understood to be a difference of at least 2 AIC points, then that variable contributes significantly to predicting crime rates.

A Swiss public transit police car. Photo by Kecko.

It turns out that all the variables I considered make a significant difference in a multiple linear regression model trying to predict Swiss crime rates. But they aren’t equally important. Removing unemployment from consideration made a difference of 4.9 AIC points, removing the percentage of foreigners made a difference of 5.9, and removing the percentage of people using mass transit made a difference of 13.6. But removing the number of citizens made a difference of 92.9 points—an order of magnitude bigger difference than the other variables.

So it looks like the strongest pattern in Kümmerli’s data is just the effect of larger communities—they have more crime.

This is not what we scientists call a “surprise.”

Moreover, it’s not particularly informative for the purpose of the question Kümmerli sets out to answer—we don’t really know how population size actually relates to humans’ tendency to be less “cooperative,” or to need police to make them cooperative. Larger population does seem to be related to more crime, but it’s also related to more mass transit use—and mass transit use strikes me as a pretty cooperative behavior.

Admittedly, that’s a pretty off-the-cuff assessment based on a couple hours of fiddling around with simple statistical analysis of an easy-to-access public data set. But I strongly suspect that you could say exactly the same thing of Kümmerli’s paper. ◼


Kümmerli, R. (2011). A test of evolutionary policing theory with data from human societies. PLoS ONE, 6 (9) DOI: 10.1371/journal.pone.0024350

Passwords and eviction notices: How do plants keep their bacterial partners honest?

The nodule-y roots of a soybean plant. (Flickr: Pro-Soil AG Solutions)

ResearchBlogging.orgNitrogen is one of the elemental building blocks of life as we know it—it’s a basic component of amino acids, which are in turn the building blocks of proteins, which form the building blocks and moving parts of every living cell. The nitrogen interwoven in our tissues originated as part of the atmosphere we breathe, but the path from atmosphere to living flesh is far less direct than drawing a breath. Atmospheric nitrogen becomes useful to us animals only via an intimate relationship between a plant and bacterial growing in its roots.

The bacteria, called rhizobia, have the rare ability to “fix” free-floating nitrogen into biologically useable form. In return for this nitrogen source, the host plant allows the rhizobia to infect a specialized knob of root tissue, a root nodule, which it supplies with sugar for the benefit of its nitrogen-fixing guests. The plant uses the fixed nitrogen to make proteins for its own use, and anything that eats the plant afterwards benefits.

If all this sounds familiar, it’s because the interaction between plants and rhizobia is the focus of my developing postdoctoral research, and I’ve been writing about it as I’ve done more reading about it. Specifically, I’ve been interested in how plants might be able to make sure their root nodules house helpful bacteria rather than freeloaders, who enjoy the sugar supply inside the nodule without fixing nitrogen in return.

I’ve discussed a couple of different mathematical models that suggest some options. However, models are really just formal ways to follow through the implications of a particular idea, not necessarily descriptions of what actually transpires between a plant and the rhizobia inside its roots. So I thought it might make sense to step back and survey what we presently know about what goes on inside those root nodules.

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