In which I try to explain why “heritability” is not quite the same thing as “heritable”

ResearchBlogging.orgRobert Kurzban responds in the ongoing “adaptive” homophobia kerfuffle (henceforth, the O.A.H.K.) with continued confusion about how biologists identify possible adaptations and test to see whether natural selection is responsible for them. He notes that one effect of natural selection is to remove heritable variation in traits under selection, so that many traits which are probably adaptations—arguably, sometimes the best-adapted traits—actually have zero heritability.

This is true. But it’s important to note that a trait having zero heritability, or no genetic variation, is not the same thing as that trait not being heritable, or having no genetic basis. If the trait has zero heritability, the observed variation in the trait may not be heritable, but the trait still may be. Kurzban’s confusion over this distinction may be a fault of the terminology, as was pointed out to me in a couple independent conversations following the last round of the O.A.H.K.

That aside, reduced heritable variation in a trait—relative to appropriate standards for comparison, like other traits in the same species or the same trait in closely related species—is sometimes used to infer that selection has acted on that trait in the past. This is what my lab has done in the case of Joshua tree and its pollinators, which Kurzban cites. This sort of approach provides only indirect evidence of natural selection’s activity—but it’s often the best you can do when your focal species isn’t amenable to growing in a lab or greenhouse within the span of a single grant cycle.

The two varieties of Joshua tree, because apparently these are part of the discussion now. Photo by jby.

The comparison to other traits or to other species is the critical point here. Without it, you can’t determine whether a lack of genetic variation is due to strong selection, or due to the fact that there is no genetic basis for the trait. In isolation, the observation that there is no heritable variation for a single trait or behavior in a single species doesn’t tell you much except that natural selection cannot currently be acting on the observed range of variation in that trait. If there’s no genetic basis for the trait at all, then it cannot have been under selection in the past, either.

Forming hypotheses versus testing them

Regarding Kurzban’s broader point about how biologists identify adaptations:

Futuyama’s textbook, which Yoder cites for the discussion of heritability, indicates the following: “Several methods are used to infer that a feature is an adaption for some particular function” (p. 261), and lists the criteria that evolutionary psychologists rely on, including complexity, evidence of design, experiments, and so on. From the material I quoted in my prior post, it seems to me that by indicating the two kinds of evidence that are necessary for inferring a feature is an adaptation, Yoder is rejecting Futuyama’s claim that one can infer adaptation from its form, complexity, and so on.

Here Kurzban is confusing how we initially infer that a trait or behavior might be an adaptation with how we actually demonstrate that a trait or behavior is an adaptation. Forming a hypothesis is not the same thing as testing it, as Jon Wilkins explained so well. If Kurzban is accurately representing evolutionary psychology’s standards of evidence, then he’s confirmed Wilkins’s accusation that evo psych usually doesn’t go beyond the step of forming a plausible hypothesis to collecting the data that can test it.

Demonstrating that an adaptive hypothesis is well supported by data is, as I’ve previously said, a lot of work—usually enough for more than one scientific article. Depending on what is easiest to do, building the case that a trait is an adaptation might start with a paper that merely demonstrates a trait’s function—but that trait has not been conclusively shown to be an adaptation until we know that its demonstrated function is selectively important, and that the trait itself has a genetic basis.

While familiar to anyone who reads the evolutionary biology literature, this maybe isn’t so obvious to non-biologists. This may be because popular science accounts don’t always differentiate between hypotheses with good scientific support and those with none. Walk through a zoo or a natural history museum, and you’ll read nothing but adaptive hypotheses all day—but you’ll rarely see good, deep discussion of how well they’re supported.

This is why, since I started graduate school, I’ve became rather tiresome company on trips to museums and zoos. But one of the great things about popular writing by working scientists (from my perspective as a scientist) is that it lets specialists explain exactly such finicky details of our fields directly to the public. Doing so clearly and accessibly is challenging, to be sure, but naïve, uncritical endorsements of unsupported hypotheses—about the adaptive values of human behavior, or anything else—are available in just about every major media outlet. If scientists don’t do better than that in our own science communication, what value do we have to add to the discussion?

And now something new: relevant data

Your reaction to this image might be in your genes, but the evidence is that it can change, too. Photo source unknown, presumed public domain.

Which brings us back to evaluating Gordon Gallup’s “adaptive” homophobia hypothesis. Kurzban also points to evidence (ye gads! data!) that natural selection actually could have something to work with in the case of attitudes towards homosexuals. A 2008 Australian twin study, which finds a genetic component of variation in responses to a questionnaire about attitudes towards homosexuality.

This is indeed, as Kurzban suggests, preliminary data in support of the idea that natural selection could operate on homophobia. As Neuroskeptic pointed out in the comments on my last O.A.H.K. post, it also means that natural selection could be operating on tolerance of homosexuals. It’s an interesting and important question, actually, why the authors of that study chose to frame their results as showing the heritability of intolerance, rather than the heritability of tolerance.

However, as I noted all the way back at the beginning of the O.A.H.K., we also know that homophobic attitudes can change considerably over the course of an individual’s lifetime. It’s hard to say how survey responses taken at a single point in time relate to what natural selection would actually have to work with, if homophobic attitudes or lack thereof somehow shape an individual human being’s expected reproductive fitness. Even if there is some solid genetic basis to homophobia, we still don’t have data that can rigorously determine whether or how natural selection might act on that variation.

References

Godsoe, W., Yoder, J.B., Smith, C.I., Drummond, C., & Pellmyr, O. (2010). Absence of population-level phenotype matching in an obligate pollination mutualism Journal of Evolutionary Biology, 23 (12), 2739-2746 DOI: 10.1111/j.1420-9101.2010.02120.x

Verweij, K., Shekar, S., Zietsch, B., Eaves, L., Bailey, J., Boomsma, D., & Martin, N. (2008). Genetic and environmental influences on individual differences in attitudes toward homosexuality: An Australian twin study. Behavior Genetics, 38 (3), 257-265 DOI: 10.1007/s10519-008-9200-9

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In which several evolutionary psychologists still don’t understand evolution

ResearchBlogging.orgJesse Bering has responded to criticism—by me, Jon Wilkins, and P.Z. Myers, among others—of his post about Gordon Gallup’s hypothesis that fear of homosexuals is favored by natural selection, in the form of an interview with Gallup. The result is informative, but probably not in the way intended.

To recap: Gallup proposed that homophobia could be adaptive if it prevented gay and lesbian adults from contacting a homophobic parent’s children and—either through actual sexual abuse or some nebulous “influence,” making those children homosexual. In support of this, he published some survey results [$a] showing that straight people were uncomfortable with adult homosexuals having contact with children.

I pointed out that all Gallup did was document the existence of a common stereotype about homosexuals—he presents no evidence that believing this stereotype can actually increase fitness via the mechanism he proposes, or that it is heritable.

Homophobia. And, um, everyone-else-phobia, too. Photo by yksin.

So now Gallup and Bering have responded, although they have not, I think, improved their case. There’s a lot for me to address here, so I’ll try to break it up into sections, and follow the order of the interview.

In which Gordon Gallup is not a homophobe

In the response post, Gallup (and Bering, who contributes quite a lot to the argument in his role as interviewer) takes issue with the collective objections of working biologists, but manages not to actually address those objections. Bering starts the conversation on the moral high ground:

BERING: Let’s address the elephant in the room. It’s embarrassing for me to even ask this of you, since the answer is so obviously “no” to me. Is your theory a justification of your own homophobia?

GALLUP: A lot of people think that if a person has a theory it’s a window unto their soul. I have lots of theories. (See CV (pdf).) I have a theory of homophobia, I have a theory of homosexuality, and I have a theory of permanent breast enlargement in women, just to mention a few. So that would make me a homophobic, homosexual who is preoccupied with women’s breasts.

Neither I, nor any of the other critics I’ve seen have called Gallup a homophobe. He may be uniquely bad at understanding how societal homophobia nullifies his interpretation of his survey results, but that doesn’t make him a homophobe. Thanks for clearing that up, though, guys.

Gallup then demonstrates that he either hasn’t actually read any of the latest criticism, or has missed the point entirely:

… It is interesting how my critics tip-toe around the fact that my approach is based on a testable hypothesis, and how they go out of their way to side-step the fact that the data we’ve collected are consistent with the predictions. Whether it is politically incorrect or contrary to prevailing social dogma, is irrelevant. In science, knowing is preferable to not knowing. Minds are like parachutes, they only function when they’re open. If I were a homosexual, I’d want to know about these data.

I certainly didn’t tiptoe around the testability of Gallup’s hypothesis—I wrote that (1) the data he presented do not test his hypothesis, and (2) the data we do have regarding the probable fitness benefits of homophobia and its heritability contradict his hypothesis. I’m entirely prepared to revise my conclusions given new data, but Gallup doesn’t have any.

In which at least one of us doesn’t understand heritability

In his next question to Gallup, Bering accuses me of “bungling” the definition of heritability, linking to evolutionary psychologist Rob Kurzban, who says that my brief definition of heritable as “passed down from parent to child more-or-less intact” is wrong because heritability is actually “the extent to which differences among individuals are due to differences in genes.”

Wow, dude. You are aware that what you just said means exactly the same thing as what I originally said, right?

Let’s go to the textbooks that Kurzban says I’m contradicting. Here’s the passage on heritability from Douglas Futuyma’s gold-standard undergraduate textbook Evolution (page 209):

One way of detecting a genetic component of variation, and of estimating VG [trait variation attributable to genetic differences] and h2 [the proportion of total trait variation explained by genetic variation], is to measure correlations* between parents and offspring, or between other relatives. For example, suppose that in a population, the mean value of a character in the members of each brood of offspring was exactly equal to the value of that character averaged between their two parents (the MIDPARENT MEAN) (Figure 9.20A). So perfect a correlation clearly would imply a strong genetic basis for the trait. [Bold text and bracketed notes mine; otherwise sic.]

The asterisk in that quote leads to a footnote pointing out that regression, rather than correlation, is more typically used. This is the definition of heritability that I learned in my undergraduate and graduate courses. It’s also the definition I’ve just helped teach to a class of third- and fourth-year undergraduate biology students in my capacity as a teaching assistant on a course in population biology.

In non-statistical terms (the kind I try to use on this blog), a positive regression between a parent’s traits and those of their offspring means, in fact, that the parent’s traits are passed on to their offspring, um, more-or-less intact.

Parent-offspring regression is widely used to estimate heritability [PDF], but you can also do similar analyses using trait measurements for siblings, or multiple generations on a pedigree. In all of these cases, known parental or sibling or familial relationships are proxies for genetic similarity—you can estimate heritability without knowing anything about specific genes. (In fact, sometimes biologists use genetic data to reconstruct pedigree relationships, then estimate heritability from the pedigree.) As implied in the quote from Futuyma’s textbook, this approach is statistically equivalent to showing that there is a significant portion of trait (phenotype) variation explained by genetic variation—which is where Kurzban seems to have become confused.

Wild parsnip, mostly here to break up the wall of text. Photo by Bas Kers.

Here’s a specific example near and dear to my field of study, species interactions: To determine whether parsnip webworms could be under natural selection to resist nasty chemicals produced by their food plant, the wild parsnip, May Berenbaum and Arthur Zangerl estimated the genetic component of variation [$a] in the worms’ capacity to choose food with lower levels of the toxins, and to tolerate the toxins they did eat. To do this, they raised webworm larvae of known parentage in the lab, and tested them on controlled diets. Their actual statistical analysis tested for an effect of the worms’ sibling relationships (parentage) on their ability to avoid toxins and survive them.

In all of Gallup’s lengthy response to Bering’s question about heritability, he doesn’t say a word about this kind of data with regard to homophobia. That’s because it doesn’t exist, and, as far as I can tell from the interview, he has no intention to try and collect it. To be completely fair, it’s harder to collect heritability data on humans than on webworms—but it’s hardly impossible. As Gallup notes, there are studies documenting heritability for, of all things, human grip strength [PDF].

Kurzban’s critique is correct in one very specific regard, which Bering doesn’t touch on. It is relatively difficult, both for logistic and resource-related reasons, to estimate a trait’s heritability and determine whether natural selection is acting on it within the same study. (Although there are plenty of exceptions—here’s one example [$a] pulled at random from my reference library.) That’s why I said, in my original post, that biologists expect evidence for heritability or fitness benefits in support of an initial claim that a trait or behavior is adaptive. The study I cited as an example of support for adaptation—which shows that horned lizards’ horns prevent predator attacks [PDF]—demonstrates fitness benefits, but not heritability. This point should be familiar to anyone who regularly reads the evolutionary biology literature.

Grip strength: known to be heritable. Homophobia: not so much. Photo by West Point Public Affairs.

So, again, Gallup has no data on the heritability of homophobia. The rest of his interview shows that he still doesn’t have any data to demonstrate fitness benefits for it, either.

In which evidence of fitness benefits also remains absent

Gallup then comes to the question of whether a child who would otherwise be straight can be “converted” to homosexuality by early same-sex sexual contact.

As detailed in my 1996 reply to Archer, we’ve collected data from male homosexuals that show that most gay males don’t report getting a clear sense of their homosexual orientation until they have their first same-sex postpubertal sexual experience.

Most gay men don’t know for sure that they’re gay until they’ve actually, you know, tried gay sex? Quelle surprise. This is absolutely classic mistaking of correlation for causation, and it suggests that Gallup doesn’t know much about the actual experience of sexual minorities. When you grow up surrounded by straight people, it often takes very direct evidence to convince you that you’re attracted to people of the same sex. If same-sex activity shortly after puberty can cause homosexuality, wouldn’t parents be most concerned about homosexuals having contact with teenagers? At the risk of sounding like a broken record, this is yet another thing we can’t tell from Gallup’s survey data—he asked about pre-pubescent children, and in one case 21-year-old children, but not children who have just passed puberty.

Finally, Gallup deals with the relative risk that homosexuals will molest children. He does this by moving the goalposts for pedophilia:

There is also evidence that shows that the propensity to have sex with minors is positively correlated with promiscuity among homosexual males. Unlike heterosexual pedophiles, homosexuals who have sex with minors target young postpubertal victims.

That’s not pedophilia Gallup is talking about—that’s violation of age-of-consent laws. The comparison between heterosexual-identified pedophiles, who target children, and homosexuals who have sex with post-pubertal teens under the age of consent is, frankly, intellectually dishonest. By definition those are two different groups. The comparison to make is that between all homosexuals who have had sex with minors and all heterosexuals who have had sex with minors. I would imagine that, as Gallup basically admits in his next sentence, those two groups look much more similar.

So that’s where we stand: still no evidence that homophobia is heritable, and still no evidence that it provides a fitness benefit by preventing the homophobe’s children from becoming homosexuals. Gallup’s only data are still, over fifteen years after his initial publication, a set of survey responses that are consistent with any number of hypotheses for the origins of homophobia. Claiming that those data demonstrate an adaptive function for hatred of homosexuals doesn’t just fail the standards of evidence for evolutionary biology, it’s bad scientific reasoning.

In which we come to a conclusion of sorts

In a coda to the interview, Bering accuses me and his other critics of failing to engage with Gallup’s results. I think my previous discussion, and Bering’s response to it, speak for themselves. Bering has demonstrated to me that he doesn’t understand undergraduate-level biology, and that, as Will Wilkinson suggested, he’s more interested in ginning up controversy than scientific rigor. (On which point he wins, I suppose. D&T’s visit count went through the roof when P.Z. Myers linked here.)

Bering also makes some conspicuously uninformed speculations about my own experience and motivations. I won’t dignify that with a response except to say yes, Jesse, I’m gay, and you don’t know the first thing about what I have or haven’t encountered in the way of “palpable disapproval.” First and foremost, though, I’m a scientist. Contrary to what you seem to think, I love a good counterintuitive, paradigm-shifting hypothesis, but I also expect it to be supported with data.

Bering, however, is convinced that he’s established himself as a hard-nosed scientific iconoclast in opposition to all us stodgy, dogmatic, evidence-demanding biologists. He concludes,

So, I’ll continue to dredge up any old theory, no matter how meager the supporting data …

Clearly, Jesse, I can expect nothing more of you.

References

Arden, N., & Spector, T. (1997). Genetic influences on muscle strength, lean body mass, and bone mineral density: A twin study. Journal of Bone and Mineral Research, 12 (12), 2076-2081 DOI: 10.1359/jbmr.1997.12.12.2076

Berenbaum, M., & Zangerl, A. (1992). Genetics of physiological and behavioral resistance to host furanocoumarins in the parsnip webworm. Evolution, 46 (5), 1373-84 DOI: 10.2307/2409943

Young, K. (2004). How the horned lizard got its horns. Science, 304 (5667) DOI: 10.1126/science.1094790

Campbell, D. (1996). Evolution of floral traits in a hermaphroditic plant: Field measurements of heritabilities and genetic correlations. Evolution, 50 (4), 1442-53 DOI: 10.2307/2410882

Futuyma, DJ. (2005). Evolution. First ed. Sunderland, MA: Sinauer Associates. Google Books.

Gallup, G. (1995). Have attitudes toward homosexuals been shaped by natural selection? Ethology and Sociobiology, 16 (1), 53-70 DOI: 10.1016/0162-3095(94)00028-6

Mousseau, T., & Roff, D. (1987). Natural selection and the heritability of fitness components. Heredity, 59 (2), 181-97 DOI: 10.1038/hdy.1987.113

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The evolution of homophobia, continued

On Twitter, hectocotyli just pointed me to another discussion of the problems with Gordon Gallup’s case for an adaptive function to homophobia (and linked to my take in connection, for which, thanks). Jon Wilkins goes into more detail on the general problem that evolutionary psychology too often accepts plausibility as the standard of proof for adaptive hypotheses.

In fact, it is trivially easy to come up with a plausible-sounding evolutionary argument to describe the origin of almost any trait. More importantly, it is often just as easy to come up with an equally plausible-sounding argument to describe the origin of a hypothetical scenario involving the exact opposite trait.

I think Wilkins is a little too polite in some regards; Gallup’s hypothesis doesn’t even qualify as “plausible” in the context of what we know today about its ugly component assumptions. (And what, by the way, Jesse Bering should have known before dredging up Gallup’s articles from well-deserved obscurity.) Nevertheless, Wilkins broadens the discussion to address scientific reasoning more generally, and the post is worth reading in its entirety.

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An adaptive fairytale with no happy ending

ResearchBlogging.orgThe evolution of human traits and behaviors is, as I’ve noted before, a contentious and personal subject. This is enough of a problem when there’s some data to inform the contentiousness. In the absence of meaningful data, it’s downright dangerous.

Take, for instance, Jesse Bering’s recent post about the evolution of homophobia, which Steve Silberman just pointed out to me.

A grim fairy tale indeed. Photo by K Wudrich.

When evolutionary biologists say a trait or behavior is “adaptive,” we mean that the trait or behavior is the way we see it now because natural selection has made it that way. That is, the trait or behavior is heritable, or passed down from parent to child more-or-less intact; and having it confers fitness benefits, or some probability of producing more offspring than folks who lack the trait. Lots of people, including some evolutionary biologists, speculate about the adaptive value of all sorts of traits—but in the absence of solid evidence for heritability or fitness benefits, such speculation tends to get derided as “adaptive storytelling.”

Evolutionary biology wasn’t always so rigorous, once upon a time. Then Stephen Jay Gould and Richard Lewontin buried adaptive storytelling under an avalanche of purple prose in their landmark 1979 essay “The Spandrels of San Marco” [PDF]. Norman Ellstrand made a similar point with better humor in a satirical 1983 article for the journal Evolution proposing adaptive explanations for why children always start life smaller than their parents [PDF]. Nowadays, when evolutionary biologists want to, say, argue that horned lizards’ horns are an adaptation for defense against predators, they have to demonstrate the claimed fitness benefit [PDF].

Evolutionary psychologists, however, seem not to have gotten the memo.

Bering’s post focuses on a series of studies by the evolutionary psychologist Gordon Gallup. Gallup was interested in the question of whether there might be an adaptive explanation for homophobia—which, given the fact that many (although far from all) human cultures treat homosexuality as a taboo—is a fair question for research. He hypothesized that treating homosexuality as taboo helped to prevent homosexual adults from contacting a homophobic parent’s children, which would reduce, however slightly, the prospects of those children growing up to be homosexual, and ensure more grandchildren for the homophobe.

Gallup supported this adaptive hypothesis with … evidence that straight people were uncomfortable about homosexuals coming into contact with children [$a]. Here’s the opening sentence of that paper’s abstract:

In a series of four surveys administered either to college students or adults, reactions toward homosexuals were found to vary as a function of (1) the homosexual’s likelihood of having contact with children and (2) the reproductive status (either real or imagined) of the respondent.

If you’ve noticed that this doesn’t mention evidence of heritability or a fitness benefit to homophobia, that’s not because I left it out—that’s because Gallup’s work contains no data to support either.

What this amounts to is arguing that homophobia is an adaptation favored by natural selection because homophobia is a thing that exists.

Could a complex behavior like homophobia have a genetic basis? Sure. Homosexuality itself is a complex behavior, and it certainly does have some genetic basis. However, the fact that attitudes toward homosexuality have shifted as far and as fast as they have in the last few decades suggests that any genetic effects underlying homophobia are pretty easy to overcome. Behaviors can be inherited culturally, too, since human children learn from their parents. But—note, again, lots of change in the last thirty years or so—cultural inheritance is more fleeting and malleable than biological inheritance.

Careful, Red Riding Hood—that wolf might be gay. Photo by crackdog.

What about Gallup’s proposed fitness benefit for homophobes? Well, that would require homophobia to, you know, actually prevent homosexuality. Gallup’s argument there hangs on two distasteful assertions. First, that gay men are more likely to be pedophiles, and second, that boys sexually abused by gay men are themselves more likely to grow up gay. In spite of Gallup’s assertions otherwise [$a], we have strong evidence from multiple studies that gay men are no more likely to be sexually attracted to children than straight men.

And there is, to my knowledge, no evidence to suggest that abuse can cause homosexuality. Bering cites a recent study that does document an association between childhood abuse and later homosexuality in men. However, the study’s authors point out that, “The reason for the connection between childhood sexual abuse and same-sex partnerships among men is not clear from our findings.”

… gay men tend, on average, to be more gender non-conforming as boys (Bailey & Zucker, 1995). This tendency could increase their appeal or conspicuousness to sexual predators, which might make them more likely to be victims of abuse (B. Mustanski, personal communication, February 11, 2008). Similarly, it is possible that boys who are developing and exploring a same-sex sexual orientation are more likely to enter situations where they are at risk for being sexually abused (Holmes & Slap, 1998). [In-text citations sic]

Why on Earth would Bering dredge up Gallup’s adaptive fairytale a decade and a half after it was published, if it was baseless to begin with and no new evidence supports it? Well, according to Bering, because he’s a hard-nosed scientist who isn’t afraid to consider uncomfortable possibilities.

Sometimes, science can be exceedingly rude—unpalatable, even. The rare batch of data, especially from the psychological sciences, can abruptly expose a society’s hypocrisies and capital delusions, all the ugly little seams in a culturally valued fable. I have always had a special affection for those scientists like Gallup who, in investigating highly charged subject matter, operate without curtseying to the court of public opinion.

Of course, says Bering, Gallup’s work isn’t conclusive, but it sure would be interesting if someone tested it.

Except, when Gallup was forming his hypotheses about the evolutionary benefits of gay-hating—he first proposed the idea in a 1983 article—he was hardly thumbing his nose at public opinion. He was, in fact, giving natural selection’s approval to the prevailing ugly stereotypes about gay men. And, as any competent evolutionary biologist would recognize, he did it without a shred of relevant evidence.

References

Ellstrand, N. (1983). Why are juveniles smaller than their parents? Evolution, 37 (5), 1091-4 DOI: 10.2307/2408423

Gallup GG Jr, & Suarez SD (1983). Homosexuality as a by-product of selection for optimal heterosexual strategies. Perspectives in Biology and Medicine, 26 (2), 315-22 PMID: 6844119

Gallup, G. (1995). Have attitudes toward homosexuals been shaped by natural selection? Ethology and Sociobiology, 16 (1), 53-70 DOI: 10.1016/0162-3095(94)00028-6

Gallup, G. (1996). Attitudes toward homosexuals and evolutionary theory: The role of evidence. Ethology and Sociobiology, 17 (4), 281-284 DOI: 10.1016/0162-3095(96)00042-8

Gould, S., & Lewontin, R. (1979). The Spandrels of San Marco and the Panglossian paradigm: A critique of the adaptationist programme. Proc. Royal Soc. B, 205 (1161), 581-98 DOI: 10.1098/rspb.1979.0086

Wilson, H., & Widom, C. (2010). Does physical abuse, sexual abuse, or neglect in childhood increase the likelihood of same-sex sexual relationships and cohabitation? A prospective 30-year follow-up. Archives of Sexual Behavior, 39 (1), 63-74 DOI: 10.1007/s10508-008-9449-3

Young, K., Brodie, E.D., Jr., & Brodie, E.D., III (2004). How the horned lizard got its horns. Science, 304 (5667) DOI: 10.1126/science.1094790

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Principle interviewee: Erica Bree Rosenblum

This post was chosen as an Editor's Selection for ResearchBlogging.orgSince her office is just down the hall from mine, I couldn’t very well write about Erica Bree Rosenblum’s latest scientific paper without talking to her about it in person. Rosenblum and her coauthor Luke Harmon weave together the stories of three lizard species’ evolutionary responses to the gypsum dunes of White Sands, New Mexico. As Rosenblum told me in our interview, the study both consummates work she began as a doctoral student and suggests new avenues of study at a striking and beautiful field site.

Erica Bree Rosenblum at White Sands, where she has studied lizards’ adaptation to the dramatic gypsum dunes since graduate school. Photo courtesy Erica Bree Rosenblum.

(I’ve edited the transcribed interview for clarity and length, and paraphrased the questions I asked in person to minimize my interruptions. Rosenblum previewed, corrected, and approved the text of her answers and my questions as they appear below.)

Jeremy B. Yoder: Tell me about the new study and its context.

Erica Bree Rosenblum: Some of the things that are compelling about White Sands that motivated us to write the “Same Same but Different” [$a] are that there are a number of different species that colonized this recent formation. … At first blush, this system looks all “same same.” You look at the main trait that has allowed these animals to survive there, which is becoming light in color, and many diurnal animals at White Sands are white, unless they have some other strategy for avoiding predation. … So a lot of my work over the last several years has been focused on the “same same” aspect of convergent evolution and on the one trait that appears to be the key trait for colonizing, which is light color.

The motivation of this paper was that there is an enormous “but different” side to the story, because there are three lizard species there, and they exhibit some really compelling differences in their degree of adaptation and their progress toward speciation. And also if you start looking at other traits besides color, if you take a multidimensional perspective on adaptation, then there are a lot of really striking differences across species.

JBY: Body size and limb length?

EBR: Body size and limb length and also the genetic basis of color and how structured the populations are across the ecotone. [The transition zone between white sand dunes and dark soil – JBY] So the motivation for this study was to look at what are the essential factors for ecological speciation and then what are the promoting factors for ecological speciation and how might the three species differ.

JBY: How did you start studying the White Sands lizards in the first place?

EBR: I was co-advised in graduate school by two eminent evolutionary biologists who have opposite perspectives on how you find study systems. My first year in graduate school, my one advisor, Craig Moritz, said to pick the theory you are interested in first and then find the system that will let you address that theory. My other advisor, David Wake, said to pick something that you love aesthetically, and then learn more about that. So I had these competing influences, in that sense, when I was trying to form my dissertation project.

Rosenblum and her collaborator Luke Harmon pursue Sceloporus magister, a close evolutionary relative of one species that has colonized White Sands. Photo courtesy Erica Bree Rosenblum.

I had just come back from a bunch of years abroad, and I knew I didn’t want to do research overseas. I also knew that I wanted to do my own thing and just “plug into” a system that had already been established. So I had an idea for wanting to do a study about ecotones—to study divergence with gene flow—in herps. [Lizards and snakes – JBY]

I had talked with different people and taken a map of the U.S. and circled every place that had really sharp transition zones that had to do with interesting problems in herpetology. So I had considered other field sites—in some of the lava flows in California that have strong transition zones, coastal-to-inland [transitions], these cool legless lizards in California—there’s a bunch of strong ecotonal transitions in western U.S. reptiles.

So I circled a bunch of places on the map and I was driving around catching animals and thinking about what I wanted to do. And when I got to White Sands, the Dave Wake part of me was drawn to it aesthetically. … It just seemed like such a striking example of adaptation with such clear possibilities. I knew I wanted to study something simple enough to wrap my head around, and White Sands has a striking, small, depauperate community, so you can actually study everything. And with a few exceptions, no one had done any biological research at White Sands since the forties, when the White Sands species were described.

JBY: What question would you like to have answered five years from now?

EBR: One of the big things I’d like to know is about the dimensionality of selection in the wild. We have a tendency to think about whatever trait seems most accessible to us, but when environments change, organisms are confronted with a lot of adaptive problems to solve at once.

… Number one is understanding the genetic architecture of adaptation and speciation. We know a lot about genotype to phenotype connections in natural populations, but we don’t know a lot about genotype-to-phenotype-to-speciation connections. I’m really interested in traits that might function as “magic traits,” that make speciation easier. I’m interested in whether [for White Sands lizards] color serves as a magic trait and can “high-tail” populations towards speciation.

The other thing I’m interested in is the genetic architecture of multidimensional adaptation. If you have lots of traits that are changing in a new environment, and it is happening very quickly over time, are the genes that underlie those adaptive traits all clustered in the genome? Is there a “signature” of multidimensional adaptation at the genetic level?

And then the third thing is about the predictability of evolution in general. I think it would be really fun to do a more systematic study of the entire fauna at White Sands and understand not just three lizard replicates but all the other species that are white, from invertebrates to mammals, to understand how predictable those adaptive changes are.

Different shades of Sceloporus undulatus, one of the three lizard species adapted to life at White Sands. Photo courtesy Simone Des Roches.

JBY: What about ten years from now?

EBR: The challenge of working at White Sands is that it’s a compelling empirical system to test some classic population genetics ideas, but it’s very hard to develop general conclusions from one system with three replicates. It’s nice to have the three lizard replicates, but it’s still only one system in one place. I’ve tried to visit all the other gypsum sand dune systems in the world. There are others—in Texas, in Mexico … they have unique faunas in other ways, but none of them seem to have blanched species. So when you study natural systems, finding compelling evolutionary replicates can be difficult.

JBY: And when we go looking for study systems we often find the ones with the strongest signals first.

EBR: That’s right … Another example where we’re running into a problem is that … in two of the three species the gene that controls color is the same gene, but has different dominance patterns [PDF]. In one species the mutation that leads to white color is recessive and in the other it’s dominant. And there’s a longstanding debate from Haldane, of how dominance should influence adaptation, but it’s just an N of two. So we could get any pattern. We’re doing follow-up studies to see if the predictions would be upheld in terms of how dominance affects the rate at which adaptive alleles are fixed, and visibility to selection. But whichever way the story goes, it’s either the way you expect it or the way you don’t expect it, but it’s just two replicates. So that is one challenge of studying things in nature.

JBY: Let’s conclude with an outrageous, blog-oriented question: Is White Sands the new Galapagos Islands?

EBR: Yes. [Laughs]

JBY: That’s what I hoped you’d say.

EBR: There are things that are compelling about white sands not only for learning about evolution but also for teaching about evolution. One of the new grants I have is for integrating research and outreach there, because it’s such a compelling place to say, “this is how adaptation happens.” You can see it with your eye, and it’s exactly what you expect. We just finished helping build a new evolution museum at the visitor center at white sands. … So I think that it has cool potential for helping public education around evolution, and it’s not as expensive to go there as it is to go to the Galapagos!

References

Rosenblum, E., Rompler, H., Schoneberg, T., & Hoekstra, H. (2009). Molecular and functional basis of phenotypic convergence in white lizards at White Sands. Proc. Nat. Acad. Sci. USA, 107 (5), 2113-7 DOI: 10.1073/pnas.0911042107

Rosenblum, E., & Harmon, L. (2010). “Same same but different”: Replicated ecological speciation at White Sands. Evolution DOI: 10.1111/j.1558-5646.2010.01190.x

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For lizards on white sands, evolution doesn’t quite repeat itself, but it does rhyme

ResearchBlogging.orgSee also my interview with Erica Bree Rosenblum, the lead author of the study discussed here.

If life on Earth started over from scratch, would it eventually re-evolve the world we see today? This is the kind of question that makes for an entertaining argument over beers: “Well, without the Chicxulub impact, the dinosaurs wouldn’t have gotten out of the way for mammals.” “But dinosaurs were already turning into birds!” You might think that to resolve that argument, we’d need a second Earth and four billion years of research funding. And maybe we would, to resolve it conclusively. But sometimes nature performs a small-scale version of that kind of experiment for us.

The gypsum sand dunes of White Sands, New Mexico. Photo by Fabian A.M.

One such natural experiment is at a special site in the New Mexico desert, a patch of gypsum sand dunes called White Sands. As my University of Idaho colleagues Erica Bree Rosenblum and Luke Harmon show in a paper just released online ahead of print by the journal Evolution, three species of lizards that colonized White Sands are following the same evolutionary path, but in different ways and at different paces [$a]. In the words of a Thai expression Rosenblum and Harmon choose to describe their thesis, the three lizards are “same same but different.”

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Is female orgasm adaptive? Let’s ask the clitoris.

Correction, 22 December 2010: Vincent Lynch, author of the second paper discussed in this post, notes in the comments that he didn’t actually conclude that female orgasm was an adaptation. I’ve corrected the post accordingly.

ResearchBlogging.orgWhether or not a trait is an adaptation, shaped by natural selection for a specific function, can be a surprisingly contentious question in evolutionary biology. When the trait in question belongs to human beings, though, “contentious” reaches a whole new level—because when evolutionary biologists consider humans, their conclusions get personal.

Erotic sculpture on temple wall, Khajuraho, India. Photo by Abhishek Singh aka Bailoo.

Among the myriad traits and behaviors of Homo sapiens evolutionary biologists might choose to study, few can be as personal as the female orgasm. The adaptive function of male orgasm is about as clear-cut as possible—it’s a mechanistic necessity for uniting a sperm with an egg. But while female orgasm is enjoyable (or so I am told; this is as lousy a point as any to admit that my expertise in this phenomenon is purely academic), it isn’t necessary for fertilization. No man can be a father without having had at least one orgasm, but a woman could conceivably give birth to a huge family without having any.

To explain the existence of female orgasm in an evolutionary context, then, biologists have two options: (1) discover a way in which female orgasm shapes reproductive success indirectly, or (2) conclude that female orgasm isn’t an adaptation. Possibilities advanced for the first option range from the benefits of closer bonding with a mate—sex is, after all, about more than mere reproduction—to suppositions that the contractions associated with orgasm help draw semen into a woman’s reproductive tract.

The argument in support of non-adaptive female orgasm takes a developmental perspective: that female orgasm is really male orgasm, as experienced in a female developmental context. That is, women have orgasms for the same reason men have nipples—because the anatomies of both sexes are constrained by their origins in the same underlying developmental program. If this is the case, natural selection would work to optimize male orgasm, without necessarily affecting female orgasm—and that suggests a way to test whether female orgasm is an adaptation.

Natural selection removes less-fit versions of traits from a population—making that trait less variable within the population under selection. Traits that don’t affect survival or reproductive success, on the other hand, are free to accumulate variation via mutation. So non-adaptive traits can be identified by comparing their variation to traits with known adaptive functions.

Who cares what natural selection thinks, anyway? Photo by JorgeMiente.es.

Psychologist Kim Wallen and philosopher of science Elisabeth Lloyd (who had advanced the hypothesis that female orgasm is non-adaptive in a 2005 book) made just such a comparison in a 2008 study. Variation in female orgasm would be challenging to measure, so they used the clitoris as an anatomic proxy. This let them use the penis—which shares a developmental origin with the clitoris and is presumably under natural selection associated with male sexual function—as an adaptive standard for comparison. In comparison to (flaccid) penis length, Wallen and Lloyd found that clitoris length was indeed more variable [$a]. As a second control, the authors also compared variation in clitoris and penis length to variation in the length of women’s vaginas, understanding that this trait, unlike the clitoris, is important for female reproductive success. Vaginal length turned out to be about as variable as penis length, and much less so than clitoris length.

There are several objections to be made to Wallen and Lloyd’s analysis, and many were made in a response [$a] by evolutionary biologist Vincent Lynch. Lynch objected to the use of length as the focal measure for the size of the clitoris, and showed that clitoral volume was about as variable as penile volume. (I would add that the study of social insects Wallen and Lloyd cite as a precedent for their analysis isn’t actually focused on variation, but on the symmetry of traits under consideration, which is not quite the same thing.) More critically, though, Lynch points out that there isn’t any known relationship between clitoral size and ability to achieve orgasm—so the data don’t have the bearing on the question that Wallen and Lloyd assigned in the first place. Lynch concluded that female orgasm is an adaptation after all—a more conservative interpretation of his result is that we can’t answer the question by measuring clitorises.

Understanding the evolution of human sexual behaviors can help us to figure out how best to navigate the tricky business of a sexual relationship with another person—an approach most recently exemplified in the book Sex at Dawn. But we also tend to view evidence that natural selection favors a particular trait or behavior as a kind of approval, or as evidence of what is “natural.” That’s silly. Whether or not they help to make more babies, orgasms are fun, and they’re a wonderful part of our most intimate expression of affection and love. In some respects, that’s all we need to know.

References

Crespi, B., & Vanderkist, B. (1997). Fluctuating asymmetry in vestigial and functional traits of a haplodiploid insect. Heredity, 79 (6), 624-30 DOI: 10.1038/hdy.1997.208

Lynch, V. (2008). Clitoral and penile size variability are not significantly different: lack of evidence for the byproduct theory of the female orgasm. Evolution & Development, 10 (4), 396-7 DOI: 10.1111/j.1525-142X.2008.00248.x

Wallen K, & Lloyd EA (2008). Clitoral variability compared with penile variability supports nonadaptation of female orgasm. Evolution & development, 10 (1), 1-2 DOI: 10.1111/j.1525-142X.2007.00207.x

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How Wright was wrong: When is it genetic drift?

This post was chosen as an Editor's Selection for ResearchBlogging.orgScience is often said to work in three easy steps: (1) observe something interesting, (2) formulate a hypothesis for why that something is interesting in the way it is, and (3) collect more observations to see if they also support that hypothesis. Wash, rinse, repeat, and you eventually get from Newton to Einstein, from Aristotle to Darwin.

Sewall Wright, pioneer of population genetics. (Wikimedia Commons)

Except, of course, it’s never that straightforward. Sometimes scientists come up with a hypothesis without a clear-cut example to support it, and then go looking that example. Sometimes observations that support a hypothesis turn out not to, if you look closer. And—here’s the funny thing—this can even happen with hypotheses that are, in the end, pretty much correct.

In the spirit of this month’s Giants Shoulders blog carnival, which focuses on “fools, failures, and frauds” in the history of science, I’m going to recount a case in which one of the greatest biologists of the Twentieth Century was fooled by a small desert flower. Sewall Wright was no fool or failure, and he certainly didn’t commit fraud, but he does seem to have been totally wrong about his favorite example of a particular population genetic process, one he discovered. That process, isolation by distance, is widely documented in natural populations today—but it also doesn’t seem to have worked the way Wright thought it did for Linanthus parryae.

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Sex after dawn: Marriage and natural selection

ResearchBlogging.orgThe book Sex at Dawn, by Christopher Ryan and Cacilda Jethá, has had a lot of press in the last month—it first popped up on my radar with Eric Michael Johnson’s review for SEED, and then it became unavoidable (for me, anyway) when Dan Savage devoted a whole column and podcast to it. The thesis of Sex at Dawn is that early humans were highly promiscuous, and that modern expectations of monogamy are probably not consistent with our biology. I haven’t read the book yet, but the discussion surrounding it has largely missed an important detail—human evolution didn’t stop when we invented agriculture.

In fact, we’ve evolved in response to agriculture. My capacity to digest milk proteins at age 28—most other mammals lose this ability as soon as they’re old enough for solid food—is the result of natural selection acting on my northern European ancestors. Sex at Dawn coauthor Christopher Ryan acknowledges exactly this, citing the same example, in a recent response to a question on his blog. I’m not aware of a study that documents human evolution in response to marriage customs, but conveniently enough, an article in the current issue of The American Naturalist does show that a population’s marital customs can shape its response to natural selection [$a].

Vintage postcard via chicks57.

The intensity and nature of natural selection often varies with age—it’s strongest on traits expressed prior to and during the period of life when most reproduction happens, and weaker on traits having to do with life after reproduction is mostly complete.

The new paper examines the effect of marriage on this relationship between age, reproductive activity, and the strength of natural selection. The authors are able to do this thanks to church records of births (via christenings), marriages, and deaths from four Finnish towns during the nineteenth century—a deep multigenerational dataset. The society described is probably as far away from the Sex at Dawn world of communal relationships within hunter-gatherer tribes as Western society has ever gotten—the births recorded are all in the context of monogamous marriages. How monogamous these marriages actually were is debatable; this was also a world before paternity testing. But the study follows women, who would probably have had less opportunity, and certainly had less social leeway, for affairs outside marriage.

Within that society, women’s reproductive success depended strongly on their husbands’ economic status, as approximated by whether or not they owned land. Women who married landowners married almost three years earlier, on average, than those who married non-landowners (between 24 and 25 years old, compared to 27). Women who married at an earlier age generally had more children survive to age 15, the paper’s benchmark for lifetime fitness—and this effect was stronger for women who married landowners.

Vintage wedding portrait via freeparking.

This meant that the intensity of potential natural selection acting on women in the study group peaked around their 30th birthday, declined slowly for around a decade, and then dropped off sharply. By comparison, an estimate of selection intensity based only the women’s probability of survival to a given age (i.e., without accounting for the need to marry before having children) just shows a steady decline with age. So marriage customs probably shaped the way natural selection could act on this population. (The comparison made, though, is a pretty facile one. I’d love to know what the intensity of selection looks like under other post-agricultural mating systems like, say, polygyny.)

Does that mean that these nineteenth-century Finns were evolving in response to the strictures of monogamy? Not necessarily. This study only estimates how strong selection would be on a trait relative to the age at which it’s expressed. That is, traits that reduced (or improved) a woman’s ability to bear children would be more strongly selected against (or favored), if they were expressed while she was between the ages of 30 and 40.

So the fact that marriage customs shape natural selection doesn’t mean that we’ve evolved to be better adapted to current marriage customs than we are to those of pre-agricultural hunter-gatherers. Marriage customs vary considerably among cultures, and over time—I don’t know of any culture that has maintained strict monogamy since the origin of agriculture. Even if a single culture did prefer monogamy that long, natural selection to adapt to that mating system would be working from a pool of genetic variation evolved from hundreds of generations of our earlier polyamorous lifestyle. It doesn’t matter how strongly natural selection would favor a perfectly monogamous person, if such a person doesn’t exist.

In other words, the key insight of Sex at Dawn—which is also a key insight of evolutionary biology in general—is right: What we can become is shaped by what we used to be. That’s certainly an important thing to keep in mind when considering a commitment that lasts till death do you part.

(For example, you might want to makes sure your significant other is of at least the same genus as you. I mean, talk about biological impediments.)

References

Gillespie, D., Lahdenperä, M., Russell, A., & Lummaa, V. (2010). Pair-bonding modifies the age-specific intensities of natural selection on human female fecundity. The American Naturalist, 176 (2), 159-69 DOI: 10.1086/653668

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With conspecifics like these, who needs predators?

Update, 19 July 2011: More than a year after this study was published, some important objections have been made about very basic assumptions of the experiment presented. Also, I’ve fixed the first link the original article.

ResearchBlogging.orgThere’s something special about islands. After moving to islands, plants adapted to rocky outcrops evolve to grow in rainforests and alpine meadows, and finches evolve to behave like woodpeckers. But why? Islands contain new food sources and habitats, they often lack predators, and they can provide more geographic barriers to generate reproductive isolation—to name just a few possibilities. A newly published ecological experiment now provides evidence that one group of island lizards diversfied because islands are crowded [$a].

There’s something about islands. Photo by Storm Crypt.

Diversification on islands may be related to density compensation, the frequently-observed principle that islands often support fewer species than mainland sites of the same area, but contain more individuals of each species—that is, island populations are usually at higher density than their mainland counterparts [$a]. Density compensation seems to arise both from lack of predators on islands, and because island populations have fewer competitor species. This may mean that, compared to mainland populations, island populations are under weaker natural selection from other species, and stronger selection from competition with other members of their own species.

A somewhat strained analogy

How could that difference in selective regimes spur diversification? Imagine two towns, one surrounded by other settlements, the other on its own in the middle of the wilderness. The town in densely-populated country is probably best off doing one thing well—to have, say, most of its inhabitants working at a factory making (to pick a product at random) sausages for trade with other towns. People living in this first town might want to start up a factory making a different product, but odds are good there’s strong competition from another town nearby, so it’s hard to get the new business off the ground—it’s really just better to invest in the existing factory.

On the other hand, the inhabitants of the town in a lightly-populated district might need more products made locally because it costs too much to import. A businesswoman in the isolated town is probably better off starting a factory that makes a product no-one is making locally—if sausages are already accounted for, there might be a market for (to pick another product at random) pharmeceuticals.

In this scenario, competition from outside exerts economic pressure to do one thing well; competition from within exerts pressure to do many different things. Both kinds of competition are present in each town, but outside competition is stronger in the town surrounded by other towns, and competition from within is stronger in the isolated town.

Anole vs. anole

The density compensation hypothesis proposes that something similar happens on islands. With fewer predators or competitor species, island populations are able to maintain higher densities of individuals. That increased density means that competition within the species becomse stronger, creating natural selection that favors individuals who can use new food resources or live in new habitats.

Density compensation seems likely to be responsible for the diversification of anole lizards on the islands of the Caribbean. In the course of colonizing Caribbean islands, anoles have repeatedly evolved into a handful of different niche specialists [PDF] called “ecomorphs,” ranging from “giant” species that live high in the forest canopy, to small species that can navigate and perch on fine twigs, and intermediate species that live on and around tree trunks. Anoles on the mainland of Central America are no less diverse than their Caribbean congeners, but they haven’t evolved mini-radiations of replicated ecomorphs—and their population densities are much lower than those of the island species.

Anolis sagrei, the brown anole. Photo from WikiMedia Commons.

If release from predators, and the ensuing increase in population density, drove the diversification of island anoles, then we might expect that natural selection from predators has less effect on the traits that differentiate the anole ecomorphs than natural selection from other anoles. Testing that hypothesis experimentally is ambitious to say the least, but that’s what the new study attempts to do.

The authors, Calsbeek and Cox, identified six very small, similar islands off the coast of the Bahamian island Greater Exuma, and introduced varying numbers of brown anoles (Anolis sagrei) onto them at the beginning of the summer. The islands were small enough that Calsbeek and Cox could selectively exclude birds by enclosing the islands in netting; by introducing predatory snakes onto some islands, they could then generate three selective regimes: no predators, birds only, and birds plus snakes. Before introducing them into these experimental setups, the authors measured each anole’s body size, hind-leg length, and running stamina, and marked each lizard so they could estimate selection acting on the three traits based on which lizards survived to be recaptured at the end of the season. (The experiments were carried out over two years, with both years’ results compiled at the end.)

The results suggest that competition makes a bigger difference for the experimental populations than predation—while the strength of natural selection acting on all three traits increased with the anoles’ population density, it didn’t change when predators were allowed access to the islands. If the levels of predation simulated on the micro-islands accurately reflect what anoles experience throughout the Caribbean, then the result is, I’d say, pretty good evidence that competition is the most important evolutionary force acting on island anoles.

I should note that, although Calsbeek and Cox’s raw result is suggestive, it’s not clear that their sample size is big enough to support all the statistical analyses they perform on the data. On balance, I think they deserve a lot of credit just for tackling this question experimentally.

References

Calsbeek, R., & Cox, R. (2010). Experimentally assessing the relative importance of predation and competition as agents of selection. Nature, 465 (7298), 613-6 DOI: 10.1038/nature09020

Givnish, T., Millam, K., Mast, A., Paterson, T., Theim, T., Hipp, A., Henss, J., Smith, J., Wood, K., & Sytsma, K. (2009). Origin, adaptive radiation and diversification of the Hawaiian lobeliads (Asterales: Campanulaceae). Proceedings of the Royal Society B: Biological Sciences, 276 (1656), 407-16 DOI: 10.1098/rspb.2008.1204

Losos, J. (1990). Ecomorphology, performance capability, and scaling of West Indian Anolis lizards: an evolutionary analysis. Ecological Monographs, 60 (3), 369-88 DOI: 10.2307/1943062

MacArthur, R., Diamond, J., & Karr, J. (1972). Density compensation in island faunas. Ecology, 53 (2) DOI: 10.2307/1934090

Pinto, G., Mahler, D., Harmon, L., & Losos, J. (2008). Testing the island effect in adaptive radiation: rates and patterns of morphological diversification in Caribbean and mainland Anolis lizards. Proceedings of the Royal Society B: Biological Sciences, 275 (1652), 2749-57 DOI: 10.1098/rspb.2008.0686

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