The living rainbow: A fatal flaw in a classic study of sexual selection

06 Drosophila melanogater Mating

A mating pair of fruit flies. (Flickr: Image Editor)

ResearchBlogging.orgA key component of classical sexual selection theory is the idea that males maximize their evolutionary fitness—the number of children they ultimately have—by mating with lots of females, while females maximize their fitness by selecting only one or a few high-quality partners. It’s pretty clear that this model works well for some species (like ducks), but also that there are many it doesn’t fit so well. Now it looks like one of the “classic” experimental examples of sexual selection may actually fall into the latter category.

Sexual selection was first proposed by Charles Darwin, in his 1871 follow-up to The Origin of Species, The Descent of Man, and Selection in Relation to Sex; but one of the earliest experimental tests of the model wasn’t published until 1948 [PDF]. The biologist A.J. Bateman allowed small groups of fruit flies—good old Drosophila melanogaster—containing equal numbers of males and females to mate at random, then reared the resulting eggs and reconstructed the parentage of the offspring to determine (1) the number of offspring each of the male and female parent flies had produced and (2) how many parters each parent fly had had.

How did Bateman reconstruct parentage decades before the advent of modern genetic testing? He used mutations with known, visible phenotypic effects as “markers”:

The fertility of individual flies of both sexes was measured by means of dominant marker genes. Several flies of each sex were mated together in one bottle, each fly carrying a different dominant marker gene. In this way, assuming the complete viability of all the marker genes, half the progeny of each fly could be identified.

That’s a pretty clever design given the technological limitations of the time. But it also turns out to be the fatal flaw in Bateman’s experiment.

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Nothing in Biology Makes Sense: The changing landscape of ecology and evolutionary biology

Scarlet monkeyflower, Mimulus cardinalis, is one of the new “field model organisms” developed for research thanks to advances in DNA sequencing technology—and a whole lot of work. Photo by Al_HikesAZ.

This week at the collaborative science blog Nothing in Biology Makes Sense!, guest contributor David Hembry, who’s just completed his Ph.D. in ecology and evolutionary biology, reflects on how much has changed since he started his doctoral research—in terms of methods, study organisms, and who his key collaborators are.

Some of the transformations in the field I think I could see coming. For instance, it was clear in 2005 that computational power would keep increasing, phylogenetics would be used more and more to ask interesting questions, more and more genomes would be available for analysis, and evolutionary developmental biology was on the rise. It was unfortunately also predictable that it would be possible to study climate change in real time over PhD-length timescales. And although the 2008 global financial crisis didn’t help, it was clear that funding and jobs were going to be more competitive than they had been for our predecessors.

But there were a number of things I didn’t see coming, and which have made the field look radically different than it was back in 2005.

For a detailed look at the last seven years of advances and shifts in the ways we study descent with modification, go read the whole thing.◼

The living rainbow: For the selective benefits of being gay, count your cousins

Photo source unknown, presumed public domain.

ResearchBlogging.orgThere’s some more new evidence for one of the theories as to how gene variants that make men more likely to be gay could persist in human populations in the face of their obvious selective disadvantages: the same genes could, when carried by women, lead to greater fertility.

I recently posted about a study of Samoan fa’afafine, that documented this effect; now an Italian team is reporting, in a forthcoming article in The Journal of Sexual Medecine, that they’ve found the same thing in a sample of 200-some French and Italian women [$a].

The authors interviewed women who were the biological mothers or aunts of gay men, and compared them to women who were mothers or aunts of straight men. They gave each participant a questionaire covering the key question—how many children they’d had. It also covered a sort of focused medical history, covering a slew of conditions that might have affected their fertility—anything from chlamydia infections to ovarian cysts to complicated pregnancies—and asked about their sexual behavior and history. Finally, the team gave the women in their sample a standardized personality test.

Even this relatively small sample showed the previously documented effect of shared genetics with gay men—women who had gay sons or nephews had more children than those who didn’t. Mothers and aunts of gay men also reported lower rates of medical conditions that could reduce their ability to have children. They said they’d had more partners than mothers and aunts of straight men (but this difference wasn’t statistically significant) and were also less concerned about family issues, and more likely to have been divorced. Finally, the personality test revealed that mothers and aunts of gay men were more extraverted.

That’s a big pile of factors tested, which makes me wonder about multiple testing issues with a small sample size. The study’s authors build a somewhat complicated narrative out of it all: They speculate that the same genes that make men gay make women less likely to have fertility-reducing conditions, but also more extraverted and more “relaxed” about building a family—which apparently also helps them have more children. So, okay, I guess that’s plausible given the results.

Here’s what the study doesn’t do, however: it doesn’t identify any specific genes involved in making gay men gay. It can’t actually test the hypothesis that there’s a genetic basis to same-sex attraction at all, much less the hypothesis that genes promoting same-sex attraction in men are located on the maternally-inherited X-chromosome. For those questions, you really need full pedigree data—or, better yet, lots and lots of genetic data; interviewing only female relatives isn’t remotely enough.

The text of the article doesn’t necessarily make that point as clearly as it could. The authors spend a great deal of time talking about the X-chromosome hypothesis, and though they make the requisite disclaimer in the Conclusions section—

With this type of limited data, we cannot directly derive a causal connection between the hypothetical sexually antagonistic autosomal or X-chromosome-linked genetic factors and health, behavior, and personality.

—that disclaimer elides the point that their data set can’t really test anything to do with genetics indirectly either.

The authors repeatedly describe their sample as a “pilot study,” however, so maybe something bigger, and more rigorous, is in the works.◼

Reference

Camperio Ciani, A., Fontanesi, L., Iemmola, F., Giannella, E., Ferron, C., & Lombardi, L. (2012). Factors associated with higher fecundity in female maternal relatives of homosexual men. The Journal of Sexual Medicine DOI: 10.1111/j.1743-6109.2012.02785.x

The living rainbow: In ducks and geese, do bigger eggs raise the sexual stakes?

Mandarin ducks. Photo by Steve-h.

ResearchBlogging.orgThe central idea of sexual selection theory is pretty simple: Females, who invest relatively more in making and raising offspring, have an incentive to be choosy about mating. Males, on the other hand, may be able to get away with no more investment that a squirt of semen—so they have an incentive to mate with any female who’ll have them. How widely that model applies in the animal kingdom is very much an open question, but it does make some specific predictions that can be tested in an evolutionary context.

One of those predictions is that, when relatively more resources are at stake in the process of making babies, sexual selection should be stronger. Austin Hughes, a biologist at the University of South Carolina, recently set out to test for that pattern in waterfowl [$a].

Ducks and their relatives already look like a good fit for classic sexual selection. In many duck species mating is coercive, so females have evolved maze-like reproductive tracts to slow down unwelcome penises—and males have, in turn, evolved corkscrewing penises to navigate those mazes. And in many species, the sexes have strikingly different coloration—generally thought to mean that males are vying for female attention with brightly colored plumage, while females are more concerned with staying hidden while sitting on a nest.

However, there are also plenty of waterfowl species where males and females are almost indistinguishable—think of swans or geese, especially. If sexual plumage differences are related to the strength of sexual selection, maybe that reflects differences in the sexual “stakes” at play in each species. Hughes tested this hypothesis by comparing closely related pairs of waterfowl species or subspecies.

As an index of the reproductive effort made by females of each species, he used the mass of the average clutch of eggs laid, as a fraction of the mass of the average female. He then tested whether the species in each pair whose females made the larger “investment” in reproducing was also the species in the pair with more pronounced sexual differences in plumage coloration. And this was, indeed, what he found.

So that looks like a neat confirmation for one predicted effect of sexual selection. A worthwhile follow-up might be to add male parental care—which may be, admittedly, harder to measure—into the mix. If males help feed and protect the brood (which is often the case for waterfowl), that should offset the cost of reproduction from a female’s perspective, which might also reduce the strength of sexual selection.◼

Reference

Hughes, A. (2012). Female reproductive effort and sexual selection on males of waterfowl. Evolutionary Biology DOI: 10.1007/s11692-012-9188-1

Carnival of Evolution, June 2012

Somewhere in Iceland. Photo by Stuck in Customs.

The monthly roundup of evolution-related online writing is (finally) live at Pharyngula, now that host P.Z. Myers is back from a trip to Iceland. P.Z. indulges his hominid cognitive biases by sorting the contributed links into neat, if somewhat idiosyncratic, categories: Bacteria, Plants, Charismatic Megafauna, Humans, Charismatic Organs in Charismatic Megafauna (i.e., mostly brains and penises), Theory, History, and Idiots. Take a moment to speculate as to where my own contributions were classified, and then head over to the Carnival for posts from worthier sources including Jerry Coyne, Anne Gutmann, and Arvind Pillai.◼

Nothing in Biology Makes Sense: Making sense of genome reduction

Over at the collaborative science blog Nothing in Biology Makes Sense!, guest contributor Levi Morran examines the processes by which bacteria can lose genes over generations of evolution.

In a recent paper, Lee and Marx (2012) test both how and why they observe large-scale patterns of gene loss in their experimentally evolved populations of Methylobacterium extorquens. They evolved these bacterial populations under different treatments of resource availability (realms of specialization) and found that all replicate populations adapted to their specific treatment over 1,500 generations. During experimental evolution, 80% of the bacterial populations exhibited nearly a 10% reduction in genome size, and many of the gene losses occurred in similar regions of the genome, some even across treatments.

To learn how and why those genes disappeared, go read the whole thing.◼

Second opinions, anyone?

In case you think I was kind of an asshole in my response to that study about female vulnerability and sexual explitability (and, fine, I was; but I’d like to think I was channeling my natural asshole-ness for a righteous and scientifically important cause), here are some non-scientists taking many of the same issues with that very study, and coming up with even more basic questions about its logic:

Hat tip to Eric Michael Johnson on Facebook.◼

Nothing in Biology Makes Sense: Making sense of evolving invaders

This week at the collaborative science blog Nothing in Biology Makes Sense, guest contributor Kathryn Turner discusses how evolutionary processes determine whether an introduced species becomes an invasive species.

First, most obviously, how is it that a species is able to come into a new environment that it is not adapted to, surrounded by new environmental conditions and foreign biological interactions, and thrive? Thrive so exaggeratedly, that it can out-compete and displace species which have been there for millennia, adapting precisely to those environmental conditions and biological interactions? How can an individual survive to propagate a population? How can any species accomplish this? Second, less obviously: why can’t more species do it? Humans transport animals and seeds (and spores and larvae, etc, etc) around all the time, but only 10% establish self-sustaining populations, and only 1% spread to new habitats, becoming potentially invasive; this is known as the ‘tens rule’ (Williamson 1993) – a funny ‘rule of thumb’ for which I could never quite figure out the math.

For the answers, or at least some ideas about possible answers, go read the whole thing.◼

Evolutionary psychology: A dialogue

Photo by C Simmons.

ResearchBlogging.orgA Biologist went down to the coffee shop one day, because the walk out to the edge of the University campus provided some brief respite from the laboratory. Along the way the Biologist encountered an Evolutionary Psychologist, who was also going to the coffee shop, and they fell to walking together.

As they entered the coffee shop, they found it crowded with undergraduates, for it was almost Finals Week. Accordingly, they joined the long queue of prospective customers waiting to place an order. Said the Evolutionary Psychologist to the Biologist, “My dear colleague, do you not see this crowd of fertile young people as I do, engaged in a dance of mate selection and competiton that predates our ancestors’ descent from the trees?”

And the Biologist replied, “I don’t believe that our ancestors had access to steamed milk and espresso. Or free wi-fi.”

“You are being amusingly obtuse!” chortled the Evolutionary Psychologist. “The environment may have changed somewhat since the days of our Darwinian origins, I will allow, but ova remain much dearer than sperm cells.”

“That much is certainly true,” said the Biologist. “But I am not sure how much it matters to the coffee-shop flirtations of undergraduates, almost none of which will result in procreative intercourse.”

“Ah,” said the Evolutionary Psychologist, “Perhaps this is a subject wherein my own field has surpassed the expertise of yours, my dear colleague. For instance, we have recently discovered [PDF] that men are more attracted to unintelligent, inattentive women—precisely what one would expect if men have been naturally selected to seek out easy opportunities for impregnation. And this search is doubtless underway all around us at this very moment.”

“That is a remarkable and possibly misogynistic hypothesis,” said the Biologist. “I am most curious to know how it was tested.”

“O! It was most elegantly done,” said the Evolutionary Psychologist. “Some of my colleagues simply asked a small class of undergraduate psychology students—males, of course—to examine photographs of women which were previously selected for their various appearances of vulnerability, and tell whether the photographs indicated vulnerability to sexual exploitation, suitability for a one-night stand, and suitability for a long-term relationship.”

“I see,” said the Biologist.

“Most surprisingly,” continued the Evolutionary Psychologist, “My colleagues discovered that the young collegiate males felt that women who looked drunk, or were standing in compromising postures, or indicating vulnerability in any of a dozen different ways, were both more vulnerable to sexual assault and more suitable for a brief sexual dalliance—but not more suitable for matrimony.

“So you see, my dear Biologist, it is not we Evolutionary Psychologists, who proposed the hypothesis of sexual exploitability, that are misogynists—the only misogynist here is Natural Selection itself, which confirmed our hypothesis.”

“I must beg your pardon, dear colleague,” said the Biologist, “but I am afraid I do not understand the basis for your conclusion. In order for this discovery to have any bearing on reproductive success, is it not the case that most human reproduction would need to occur via coerced intercourse?”

“I must confess that this seems to be what the data indicate,” replied the Evolutionary Psychologist. “But we must not conclude therefrom that all men are rapists! By no means, dear colleague. I think it is quite plain that this result demonstrates no more then that all men are potential rapists.”

“But I remain perplexed!” said the Biologist. “Surely rape is an inefficient way to reproduce, since babies traditionally require a good deal of care after impregnation, and women have long known how to un-plant unwanted seeds.”

“That,” said the Evolutionary Psychologist, “is an important question to be resolved by additional study! But of course it need only be the case that the occasional coercive impregnation could increase a man’s reproductive success, however slightly, for Natural Selection to grab hold.”

“I suspect,” said the Biologist, “that you attribute greater efficiency to Natural Selection than this evolutionary force truly possesses, my dear colleague. But even if drunken collegiate hook-ups were a viable avenue for procreation, you must concede that there would needs be some genetic basis for the tendency to reproduce in this fashion, if Natural Selection is to act upon it. Do you truly believe this to be the case?”

“What a peculiar question!” exclaimed the Evolutionary Psychologist. “I thought that you Biologists were well aware that, in the absence of evidence to the contrary, it is quite safe to assume that any and all aspects of human nature have a heritable genetic basis. Would you truly require the demonstration of heritability in order to conclude that an observed trait or behavior is adapted by Natural Selection?”

“Indeed we would,” said the Biologist. “Such a demonstration, in the case of a tendency to sexual coercion, would be considered most remarkable in its own right, in the scholarly journals of my discipline.”

“What a boring and backward discipline you practice!” said the Evolutionary Psychologist. “Truly, it is no wonder that your field has seen no great advance this last half-century, even as we Evolutionary Psychologists dissect the very nature of humanity.”

“Your ambitions,” said the Biologist, “are indeed remarkable.”

At this juncture, the two colleagues found that they had reached the front of the queue, placed their orders, and went their separate ways.◼

References

Goetz, C., Easton, J., Lewis, D., & Buss, D. (2012). Sexual exploitability: Observable cues and their link to sexual attraction. Evolution and Human Behavior DOI: 10.1016/j.evolhumbehav.2011.12.004

Ecological complexity breeds evolutionary complication

Photo by futureatlas.

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

It is a truth universally acknowledged in evolutionary biology, that one species interacting with another species, must be having some effect on that other species’ evolution.

Actually, that’s not really true. Biologists generally agree that predators, prey, parasites, and competitors can exert natural selection on the other species they encounter, but we’re still not sure how much those interactions matter over millions of years of evolutionary history.

On the one hand, groups of species that are engaged in tight coevolutionary relationships are also very diverse, which could mean that coevolution causes diversity. But it could be that the other way around: diversity could create coevolutionary specificity, if larger groups of closely-related species are forced into narower interactions to avoid competing with each other.

Part of the problem is that it’s hard to study a species evolving over time without interacting with any other species—how can we identify the effect of coevolution if we can’t see what happens in its absence? If only we could force some critters to evolve with and without other critters, and compare the results after many generations …

Oh, wait. That is totally possible. And the results have just been published.

A team of evolutionary microbiologists has performed exactly the experiment I outlined above. The study’s lead author is Diane Lawrence, a Ph.D. student in the lab of Timothy Barraclough, who is listed as senior author.

For the experiment, the team isolated five bacterial species, of very different lineages, from pools of water at the bases of beech trees—ephemeral pockets of habitat for all sorts of microbes that break down woody debris, dead leaves, and other detritus. They cultured the bacteria on tea made from beech leaves, in vials containing either a single species, or all five species, and let them evolve for eight weeks—several dozens of bacterial generations. In a particularly clever twist on standard experimental evolution methods, they also used nuclear magnetic resonance (NMR) to identify the carbon compounds in sterilized tea that had been “used up” by the bacterial cultures, and compared the compounds in fresh beech tea to determine what the bacteria were eating.

The base of a beech tree. Photo by -nanio-.

And, maybe not surprisingly, the bacterial species’ evolution with company turned out to be quite a bit from their evolution alone. Left alone, most of the species evolved a faster growth rate. This is a common result in experimental evolution, because the process of transferring evolving bacteria to fresh growth medium—”serial transfers” that were performed fifteen times over the course of the experimetn—can create natural selection that favors fast-growing mutants. But, grown all together in the same tube, species that had evolved faster growth rates in the solo experiment evolved slower growth instead.

To find out what had evolved in the multi-species tubes, the team tested the growth of the bacterial species on beech tea that had been used to grow one of the other species, then sterilized. The original, ancestral strains of bacteria generally had negative effects on each others’ growth—they lived on similar compounds in the beech tea, and so their used tea wasn’t very nourishing for the other species. The same thing occurred with the strains that had evolved alone, only stronger, which makes sense in light of the increased growth rates, which would’ve depleted the growth medium faster.

But the interactions among the strains of the different bacterial species that had evolved together was strikingly different. Many of them actually made the tea more nutritious for other species in the evolved community. That is, some of the bacteria had evolved the capacity to eat the waste products of another species that was evolving with them. Using the NMR method to track changes in the presence of different carbon compounds in the tea before and after use provided confirmation that the co-evolved species were using, and producing, complementary sets of resources.

In short, the evolving community didn’t simply become more diverse—it evolved new kinds of mutually beneficial relationships between species that began as competitors.

Beech leaves—yum? Photo by Colin-47.

That evolutionary shift toward mutual benefit had a significant impact on the bacterial community as a whole, too. Lawrence et al. assembled new communities of bacteria extracted from the end-point of the group evolution experiment, and compared their carbon dioxide production, a proxy for overall metabolic activity, to that of a community assembled from bacteria extracted from the end point of the solo-evolution experiments. The community of co-evolved bacteria produced significantly more carbon dioxide, suggesting they were collectively able to make more use out of the growth medium.

So that’s a pretty nifty set of results, I have to say. But I’m also left wondering what it tells us more generally. In both Lawrence et al.‘s paper, and in accompanying commentary by Martin Tucotte, Michael Corrin, and Marc Johnson, there’s a fair bit of emphasis on the unpredictability of the result. Lawrence et al. write, in their Discussion section,

The way in which species adapted to new conditions in the laboratory when in monoculture—the setting assumed for many evolutionary theories and experiments—provided little information on the outcome of evolution in the diverse community.

And, as Corrin et al. note,

These results imply that predictions constructed from single-species experiments might be of limited use given that most species interact with many others in nature.

So … evolution went differently under different conditions? That isn’t exactly a shocking revelation. The fact that this is one of the study’s major conclusions is a symptom of how little experimental work has actually tested the effects of multiple species on evolution. One experiment I’ve discussed here previously, focused on the joint effects of predators and competitors on microbes that live in pitcher plant pitfalls, similarly emphasized the fact that it wasn’t possible to predict the evolutionary effects of predators and competitors together based solely on their individual effects. Work in this line of inquiry is hanging at the point of establishing that complex conditions lead to complex results.

What I’d really like to know—and I think all the authors of both the paper and the commentary would agree with me on this—is how we can begin to make general predictions about community evolution beyond, “it depends what we put in at the start.” It may be that we’ll need a lot more studies like this current one before we can start to identify common processes, and more interesting trends.◼

References

Turcotte, M., Corrin, M., & Johnson, M. (2012). Adaptive evolution in ecological communities. PLoS Biology, 10 (5) DOI: 10.1371/journal.pbio.1001332

Lawrence, D., Fiegna, F., Behrends, V., Bundy, J., Phillimore, A., Bell, T., & Barraclough, T. (2012). Species interactions alter evolutionary responses to a novel environment. PLoS Biology, 10 (5) DOI: 10.1371/journal.pbio.1001330