Everybody wins but the short-legged anoles
This quick article by Jonathan Losos and colleagues is entirely unsurprising, but good to read:
Rapid Temporal Reversal in Predator-Driven Natural Selection
Because of its potentially epochal scope, evolutionary biology is often caricatured as a strictly descriptive science, but recent years have shown that evolution can be studied on short time scales and that evolutionary biology can be both experimental and predictive. Here, we report just such an example by demonstrating the occurrence of a predicted reversal in the direction of natural selection on limb length in Anolis sagrei, a common Bahamian lizard often found on the ground in the absence of terrestrial predators.
Previous research showed that, when a larger and entirely terrestrial predatory lizard, Leiocephalus carinatus, invades, A. sagrei becomes more arboreal and that the extent of this habitat shift broadens through time (3). Hence, we predicted that the direction of selection operating on limb length in A. sagrei would change through time in the presence of L. carinatus (4): Initially A. sagrei occurs mostly on the ground, so individuals with relatively longer legs, being faster (5), would be better able to elude the predators and thereby be favored. As A. sagrei becomes more arboreal, however, we predicted that selection would favor the reverse because shorter limbs are better suited for movement on the narrow and irregular surfaces A. sagrei would use to avoid the terrestrial predator (5).
This is quite a scenario. Long-legged lizards can run faster on the ground, so initially the short-legged lizards get eaten. But in the long term, the ground is not viable as anole habitat in the presence of predation, so over time individuals that exploit trees do better. And short legs enable them to climb better.
Sound familiar?
You may not have guessed it from the fairly anaesthetic title, but this is an experiment where they basically let the velociraptors loose:
To test this hypothesis, we introduced L. carinatus to six small Bahamian islands that naturally contained A. sagrei, randomly choosing six others to serve as controls (L. carinatus occurs on nearby larger islands and is known to colonize smaller islands); the number of L. carinatus introduced (all adults) was proportional to the number of A. sagrei resident on the island. Before introduction of L. carinatus, A. sagrei individuals on each island were measured and individually marked. Islands were exhaustively censused after 6 and 12 months to determine survival (6).
Can you imagine the look on the anoles' faces? Well, I guess lizard victims are less sympathetic. Maybe if they were birds and Bolivian tree lizards came to eat their eggs?
The bottom line of the paper is that this kind of rapid reversal can occur when behaviors are plastic -- in this case, the adoption of higher arboreality takes a while to kick in, but then selects for features not adaptive on the ground.
I wouldn't really call this case a reversal of selection, though. When the bad lizards show up, surely the subset of the anole population that was already choosing more arboreal substrates had an immediate advantage. The brief increase in leg length represents disruptive selection -- the anoles that do the worst are the short-legged terrestrial ones, and long-legged terrestrial anoles do well only so far as the short-legged ones are taking all the heat.
Still you don't run across the dynamics of disruptive selection every day.
References:
Losos JB, Schoener TW, Langerhans RB, Spiller DA. 2006. Rapid temporal reversal in predator-driven natural selection. Science 314:1111. DOI link
The expensive beetle horn hypothesis
Carl Zimmer has a great post discussing a paper by Douglas Emlen and colleagues (2005) on beetle evolution. I don't normally do a lot of beetle blogging, but this paper is a great study in evolutionary trade-offs related to sexual selection and the evolution of novel body structures.
From Zimmer's post:
The researchers proposed that growing horns would force a trade-off with other important parts of the body, such as eyes and antennae. And the beetle tree supports their proposal. It is harder for beetles to detect the odor of dung with their antennae in a pasture than in a forest, because the odor plumes last longer in the woods. Four out of the five gains of new horns took place in forestsÑperhaps because beetles could afford to grow smaller antennae in a place where smelling wasnÕt so hard. On the flip side, in seven of the nine cases in which horns were lost, the beetles became nocturnal. Beetles that fly at night need larger eyes, and so they canÕt afford to shunt resources to big horns any more. The pressure to evolve bigger horns still exists in these lineages, but itÕs been offset by other demands.
References:
Emlen DJ, Marangelo J, Ball B, and Cunningham CW. 2005. Diversity in the weapons of sexual selection: horn evolution in the beetle genus Onthophagus (Coleoptera: Scarabaeidae). Evolution 59:1060-1084. Abstract
Evolution books on the march
The New York Review of Books is running a combined review of three recent evolution books:
From DNA to Diversity: Molecular Genetics and the Evolution of Animal Design, by Sean B. Carroll, Jennifer K. Grenier, and Scott D. Weatherbee
Endless Forms Most Beautiful: The New Science of Evo Devo and the Making of the Animal Kingdom, by Sean B. Carroll
The Plausibility of Life:Resolving Darwin's Dilemma, by Marc W. Kirschner and John C. Gerhart
The review was written by Edward Ziff and Israel Rosenfeld, and it's a good long discussion of how the books fit into recent evolutionary theory, from Darwin to Hox genes.
While Carroll argues--a claim that is at the heart of Evo Devo--that embryological development gives us the deepest clues to the mechanisms of evolution, Kirschner and Gerhart move beyond embryology to show that metabolic and physiological processes are also critical to evolutionary change. Their approach, which they call the theory of "facilitated variation," attempts to show how the regulation of genes inside the embryo, as described by Carroll, is part of a larger set of processes that allow organisms to experiment with evolution in a tightly controlled way. According to this theory, the mutations, or variations, needed to drive evolutionary change can occur with little disruption either to the basic organization of an organism or to the core processes that make its cells function.
To see how they get to that conclusion, you have to read the review!
Conditional response, alternative strategies, and female orgasm
I'm trying to resist becoming a hotbed of female orgasm blogging, but I just heard a promo for the story on the local news, so it seems impossible to avoid. Moreover, the issue has become a genuinely interesting debate about the role and method of evolutionary analysis. On this, I have a small contribution to make.
The Guardian is running a story on research by Kate Dunn and colleagues (2005) into the heritability of sexual response in women. Here's the abstract:
Orgasmic dysfunction in females is commonly reported in the general population with little consensus on its aetiology. We performed a classical twin study to explore whether there were observable genetic influences on female orgasmic dysfunction. Adult females from the TwinsUK register were sent a confidential survey including questions on sexual problems. Complete responses to the questions on orgasmic dysfunction were obtained from 4037 women consisting of 683 monozygotic and 714 dizygotic pairs of female twins aged between 19 and 83 years. One in three women (32%) reported never or infrequently achieving orgasm during intercourse, with a corresponding figure of 21% during masturbation. A significant genetic influence was seen with an estimated heritability for difficulty reaching orgasm during intercourse of 34% (95% confidence interval 27-40%) and 45% (95% confidence interval 38-52%) for orgasm during masturbation. These results show that the wide variation in orgasmic dysfunction in females has a genetic basis and cannot be attributed solely to cultural influences. These results should stimulate further research into the biological and perhaps evolutionary processes governing female sexual function.
At the Philosophy of Biology weblog, Elisabeth Lloyd (author of aforementioned book on female orgasm evolution) has a post generally supportive of the paper itself, but very critical of press accounts of it. She directs her greatest criticism toward the following comments by study senior author Tim Spector, which appear in the Guardian article:
Tim Spector of St Thomas's hospital in London, who led the research, said: "The theory is that the orgasm is an evolutionary way of seeing if men can prove themselves to be likely good providers or dependable, patient and caring enough to look after the kids."
Women who orgasm very easily may be more likely to be satisfied with poor quality men.
"Perhaps women who had orgasms too easily weren't very good selectors," Professor Spector said. "It paid women to be more fussy and this is one way of doing it. The simple fact is that it takes women on average 12 minutes and men two and a half minutes to reach orgasm. Adjusting to that imbalance is a test."
Lloyd has done a lot of thinking about this hypothesis, and she has a lot of ammo to unload on it. I quote from her post to give her deconstruction with some of its original clarity:
As the Guardian article makes clear, Spector is (re-)proposing a theory that orgasm is a mate-selecting device; he claims that the fact that orgasm during intercourse is difficult to attain is an evolutionary adaptation itself, making the well-known variability in orgasm among women an adaptation.
But we run into trouble immediately. The proposed adaptive state is a conditional response to quality males - have an orgasm if he's a good guy, don't if he's not - and under this theory, clearly the population of women was under selection pressure to have moved towards that optimum peak (balanced by the usual energetic costs, and so on). So why would that be an argument for the variability of orgasmic response, and not an argument for the standard result of a directional selection regime, namely, a peak at the optimum?
She goes on to summarize the data from the study, which fairly convincingly show that all females cannot have been selected to pursue this strategy -- their variability is too extensive:
If selection has been of any appreciable strength, and has been going on at least since the advent of archaic humans, we should expect that nearly all women would have such a conditional response to intercourse, and thus that nearly all women would be capable of orgasm with intercourse under the right conditions. The bad news is that there is no evidence for such a peak at all, that a full third of women rarely or never have orgasm with intercourse, and that as many as one out of ten women don't have an orgasm even once in their lives. There is a small peak in the distribution, but it is located at the non-orgasmic segment of the distribution. In other words, this is the kind of variability he needs to support his theory, and his own data show that the supporting evidence just isn't there, as I'll detail in a moment.
But there's another kind of variability, namely, that some women never have orgasm with intercourse, some women always do, and some women sometimes do and sometimes don't. This kind of variability is the kind that they do document in their study, and this kind of variability would not be selected for under his proposed hypothesis, but perversely, he implies that it would.
Heritability and alternative strategies
But I'm not sure that Lloyd and Spector are really talking about the same hypothesis. (Disclaimer: Hey, I don't know, maybe they are, in which case Lloyd's critique is more valid than I suggest.) The prologue to the Spector quote taken from the Guardian reads as follows:
The findings suggest the failure of some women to orgasm regularly is not a dysfunction, but a sophisticated mate-selection strategy that evolved during prehistoric times.
When I read that, I believed that Spector was arguing that some women (namely the ones with rarer orgasms) may have had an adaptive strategy for conditional response to male quality, leaving unstated the obvious corollary that other women may pursue different adaptive strategies.
After all, the idea that all women follow the conditional response strategy is ridiculous on its face: it cannot explain the women who reach orgasm easily and quickly most of the time, regardless of partner. If female orgasm is an adaptation, clearly there must be at least two distinct strategies: one in which orgasm is difficult and arrived at only through certain efforts, and one in which orgasm is readily achieved. There is no reason why these alternative strategies may not competed with each other in ancient human populations, considering each may have distinct advantages and drawbacks. A quick orgasm may make sex very compelling, possibly resulting in a higher frequency of inseminations -- possibly from multiple male partners. This strategy would reduce the risks associated with partnering with a single male (especially the risk of male infertility), while increasing the genetic diversity of a woman's offspring. In contrast, the conditional response strategy might have the predicted effects in encouraging female choice for male quality. Please remember that neither of these strategies has been tested, nor has the effect of their conjunction; I merely say that the hypothesis is conceivable that both of them coexisted as genetic variants within ancient human populations.
Indeed, there is no reason why there should not have been a large number of different adapted strategies toward female orgasms in past human societies. Human sexual experience must have been highly heterogenous, and the selective consequences of partially heritable mating strategies would interact in a complex way. It has the makings of a very interesting evolutionary problem.
Now, I agree that the uncritical acceptance of these hypotheses is not warranted. And I agree with Lloyd that a nonadaptive hypothesis is also very credible. The data do not point one direction or another at this point. But it is far too soon to discount the possibility that there are multiple adapted sexual strategies in human females that incorporate orgasm in differing ways.
Considering the hypothesis of alternative strategies, Lloyd's critique is mostly hollow. Consider the following passage:
The fact that this new study establishes a heritability of .45 for orgasm with masturbation (which is much more revealing than orgasm with intercourse, as far as basic orgasmic capacity goes), is also very damaging to any adaptationist account, and I'm surprised that technical people aren't saying so. Traits that are species-adaptations, such as, for example, having the capacity for language, or starting off with a good sense of taste, or having a massive brain, have heritabilities near zero. Nearly all the variability has been used up, selected out. This is just the end result of what I've just recited about the peaks in distributions. If selection is strong enough and goes on for long enough, variability around the peak gets weeded out through selection, and we're left with just one type plus random mutation and somatic, developmental, and environmental accident. Traits with heritabilities near .5 are not even close to being decent candidates for species-wide adaptations, for just this reason, as is widely known (I thought...).
FOURTH CONCLUSION: Spector's own heritability results also indicate that female orgasm is not an adaptation. Is it only population geneticists who know that species-wide adaptations have heritabilities near zero? How can it be that an expert on heritability like Spector doesn't know this? I guess this piece of knowledge might be a casualty of over-specialization.
I guess I'm as "technical" a person as has considered the issue lately, and Lloyd is just wrong about this. Certainly it is true that Fisher's Fundamental Theorem predicts that the heritability of a trait will decrease under directional selection, but Lloyd has provided us no reason to suppose that selection on female orgasm need have been directional in its pattern. Even if it were true that female orgasm were centered around a single strongly selected peak, it is far more likely that this peak would be the product of stabilizing selection rather than directional selection. The persistence of genetic variation (and thereby heritability) in such a scenario would depend on the effects of the genes themselves (e.g., is there heterosis? epistasis? antagonistic pleiotropy?). There is no simple answer to these questions, we have no knowledge whatever about the genes influencing female orgasm, and hence, it is impossible to make categorical statements about the likely heritability of the character after a history of selection.
If, as I think is a more likely scenario, there are alternative adaptive strategies toward female orgasm in humans, then it is not only likely, but necessary that the trait have substantial heritability. Unless offspring are similar to their parents, there is no sense in which alternative adaptive strategies can exist as adaptations (although under such circumstances they may well exist as cultural strategies without necessary genetic correlates).
"Species-wide adaptations"
Likewise, Lloyd's "fourth conclusion" confusingly states that "species-wide adaptations have heritabilities near zero." Remember that heritability is simply the proportion of phenotypic variance explained by genetic variance. Heritability may be near zero if phenotypic variance is high while genetic variance is very low. It may also be near zero if phenotypic variance is very low -- if the population just does not vary in the trait under consideration.
What does Lloyd mean by a "species-wide adaptation"? This is not clear to me, because her examples clearly are different in terms of variability. Humans today universally have language, and they universally have large brains (compared to, say, chimpanzees). But while the heritability of linguistic capacity is unknown, the heritability of brain size is very high in today's humans (> 0.9). Thus, it is desirable that we should be very careful in describing a trait as a "species-wide adaptation," at least if by this we mean to include some limit to the degree of potential heritability.
The example of language would seem to imply a discrete feature that differs categorically between species. A simpler example (that does not beg the question of ape linguistic capacity) is one of the human adaptations for obligate bipedality: an adducted big toe. Almost no humans have an opposable big toe; almost no chimpanzees have an adducted one. The distribution of variation of such traits nearly completely separates different species from each other, and within a species their heritability is near zero -- because their variation is near zero.
If this is the kind of trait Lloyd refers to, then it is true but trivial that such traits have heritabilities near zero. The fact that their phenotypic variance within a species is near zero allows no other conclusion. It is equally true that if we assert that female orgasm is a "species-wide adaptation" in the sense of being categorically absent from other species, then we must conclude that its heritability within humans as a categorical trait must be near zero.
But there is no reason to think that any aspect of female (or male) sexuality is a "species-wide adaptation" like an adducted big toe. As Lloyd's example of brain size makes clear, many species-typical adaptations have substantial within-species heritabilities. For example, humans have a high valgus angle, meaning the angle at the knee joint between the long axes of the femur and tibia. This angle facilitates bipedal locomotion by placing the tibia beneath the body's center of gravity during single-legged stance. This trait is clearly species-typical: human femora can easily be differentiated from chimpanzee femora by the valgus angle. But at the same time, the valgus angle itself is variable within humans. That is to say, the distribution of this continuous variable both separates humans from chimpanzees and distinguishes humans from each other. Within humans, much of the phenotypic variance is explained by underlying genetic factors, through the phenotypic correlations with other traits, such as stature, leg length, and pelvis width. Thus, this human-specific trait is moderately heritable within humans.
Human-specific traits in which alternative strategies underlie variation likewise are extensively heritable. As a case in point, human intelligence is substantially different from intelligence in any other hominoid species. Although some (hypothetical) measurement of intelligence might show some slim overlap between humans and chimpanzees in its distribution, the mean values of the two species are so different that they defy scaling. Even so, intelligence is both substantially variable in humans and substantially heritable. This heritability of intelligence may have many causes, but one of them must be the fact that intelligence itself comprises many different mental abilities that each have separate adaptive consequences. It is widely believed that such adaptive variation may in part predispose people to differing behavioral strategies, including variation in personality.
I tend to think this is not very far from the mode of evolution of human sexuality. Dunn et al. (2005:3) in fact consider mental factors as potential behavioral mediators:
Other potentially imoprtant biological factors include androgen levels or receptors, or natural variations in pleasure centres in the brain, resulting from dopamine or other psychological mood effects. All of these processes are probably mediated to some extent by genetic variations. Other associated factors, such as differences between individuals in anxiety and depression, also have heritable components and may partly contribute to the genetic component of orgasmic ability reported here.
It seems shortsighted to consider the evolution of female sexuality in isolation from the complex neurological factors that mediate female social behavior. A low frequency of orgasm during masturbation has little meaning as an adaptive character. The response to social situations, nonsexual interactions with female peers and potential male -- and female -- sexual partners, and long-term stresses must be considered in a full account of the biology of sexuality. The story does not begin or end at the clitoris, but must ultimately focus on the human as a psychological whole.
After all, the first lesson in health class is that the most important sexual organ is the one between the ears.
UPDATE 6/10/05: Elisabeth Lloyd has been kind enough to comment on this post in the comments to her original post on the subject. This has cleared up much confusion, particularly concerning the state of adaptive hypotheses for female orgasm.
Apparently, although I would never have guessed it, my hypothesis of multiple alternative strategies is novel. It seemed almost too obvious to be worth posting to me, since most of my recent thinking has been about brain evolution where these kinds of alternative strategies are common parlance. If you are a scientist reading this, take note: this is one of the great advantages of blogging, since what seems obvious to you may not be so to someone in a different field, and vice-versa.
In her comment, Lloyd acknowledges my point that only directional selection necessarily reduces heritability, but informs us that adaptive hypotheses concerning female orgasm have been framed exclusively assuming directional selection. In this case, her arguments certainly do apply to those hypotheses. This is one of the drawbacks of contemporary adaptationism that is not included in Gould and Lewontin's classic essay, "The Spandrels of San Marco": the frequent assumption that adaptations are the result of directional selection rather than other patterns. It is also a frequent confusion as applied to Sewall Wright's concept of adaptive peaks, which are not maintained by direcional selection, nor are they necessarily reached by it.
At any rate, as I mention above, I scarcely think the hypothesis of alternative strategies is testable. By introducing the possibility of many additional parameters, the hypothesis conceivably may be consistent with almost any distribution of orgasm incidence or facility. The important question is whether the hypothesized strategies may be biologically justifiable, and this will necessarily remain an impossible question to answer as long as the other behavioral correlates of such strategies are unknown. Lloyd's comment points out the problems with some such strategies as applied to the evidence. This is a bouncing ball in a sense: whenever one strategy is demonstrated to be biologically problematic, one might still propose a different set of strategies that would be commensurate with the same observations. At some point this becomes a reductio ad absurdum, but there is little chance that even the first level of two contrasting adaptive strategies can be tested with data now available.
Also note, that the more we consider correlates of female orgasm, the more we approach a non-adaptive hypothesis. That is to say, if female orgasm depends for its frequency, pattern, and existence upon other psychological or behavioral qualities, then it is possibly much simpler to argue that it is selection upon these qualities rather than orgasm itself that has shaped its distribution.
So again, this is a very much more interesting evolutionary problem than at first it might appear, and very intimately connected to the evolutionary history of the human mind.
Many thanks to Elisabeth Lloyd for her gracious and thoughtful comment. I'll never snark about orgasm-blogging again!
References:
Dunn KM, Cherkas LF and Spector TD. 2005. Genetic influences on variation in female orgasmic function: a twin study. Biol Lett (advance online). Royal Society Publications online
Inevitable King Kong island giant story
As surely as night follows day, we have this story from CNN on the real island giant animals that evolved in a King-Kong-like fashion.
Animals sometimes follow exotic evolutionary trajectories on islands because of a lack of predators or competitors. That's the essential truth of the story. It certainly explains the killer mice:
On remote Gough Island in the South Atlantic, "monster mice" are eating albatross chicks alive, threatening rare bird species on the world's most important seabird colony.
The house mice -- believed to have made their way to Gough decades ago on sealing and whaling ships -- have evolved to about three times their normal size.
But you can't shoehorn these cases into a universal "islands breed giants and dwarfs" rule. Consider:
The huge Indian Ocean island of Madagascar -- the setting of another 2005 Hollywood blockbuster -- has also given rise to plenty of natural oddities.
These included massive elephant birds that stood over 9 feet 10 inches in height and lemurs that weighed 176 pounds and more.
Yes, and mouse lemurs, and dozens of species of every intermediate size. The point is that the island created opportunities that might have been filled by other animals in a larger landmass.
A reader sent me a reference to a 2001 PNAS paper by Gary Burness, Jared Diamond, and Timothy Flannery that examines the relation of land area to body size of top carnivores and herbivores. There's no mechanism in the paper to relate the two, but there does seem to be an empirical relationship between the areas of islands and continental landmasses of different sizes and the sizes of their largest animals.
Ectotherms in the empirical data get larger than endotherms, also. So taking everything together, there shouldn't be either dinosaurs or gigantogorillas on Skull Island, but if there were either, they should be dwarfish in size, and the dinosaurs should be plenty larger than the giant gorilla.
And of course, they shouldn't exist in populations of single individuals!
CNN has this part covered, also:
Seemingly the last of his kind, King Kong also reflects another phenomenon of islands -- their disturbingly high rate of extinction, especially when humans land on them.
Many island species have evolved in a predator-free environment -- producing things like flightlessness in birds -- which makes them easy prey for meat-eating intruders.
Such was the fate of Madagascar's elephant birds as well as the famed dodo of Mauritius.
According to the World Conservation Union, close to 800 species have become extinct since 1500, when accurate historical and scientific records began.
While the vast majority of extinctions since that time have occurred on islands, over the past 20 years continental extinctions have become as common.
Scientists say this is partly because continental habitats are being diced up by human activities -- a process that is creating what some biologists term "virtual islands."
King Kong's real-life relatives are marooned on one of these "islands" on East Africa's Virunga mountain range, home to the last of the world's roughly 700 mountain gorillas.
I think the most interesting aspect of Skull Island is the way it exaggerates the scale of the man-nature conflict. Clearly the fauna of the island could never exist. But to make a nature capable of thwarting humans, even for a short time, it takes predators of gigantic proportions. Even in 1933, the real gorillas wouldn't stand a chance.
It is notable that in later movies featuring giant animals, like Godzilla and Them, they are frequently products of human agency -- especially our abuse of poorly understood forces of nature like radioactivity.
As I write this, by the way, the television has "Speed Buggy" encountering a giant island gorilla named "King Zilla".
References:
Burness GP, Diamond J, Flannery T. 2001. Dinosaurs, dragons, and dwarfs: the evolution of maximal body size. Proc Nat Acad Sci USA 98:14518-14523. Full text
Evolution and the female orgasm
I admit, I was sucked in by a link (via kausfiles) to the Huffington Post. How snarky of me. But I couldn't resist this one:
Wouldn't it be delicious if the female orgasm were the thing that tips the scales in favor of the Intelligent Design crowd? It would make for a great closing argument: "The female orgasm is so complex and strange, it could only have come from God. The reason there is no evolutionary purpose to it is because there is no evolution!
Turns out it's a post by Arianna herself reacting to a New York Times article about Elisabeth Lloyd's new book, The Case of the Female Orgasm: Bias in the Science of Evolution. Arianna's post makes little sense of the issue, which is yet another reflection of how evolutionists manage to speak past most of the public. I'm sure there's a special joy to be found in becoming a one-liner on Letterman, but it's not exactly the pinnacle of scientific communication.
This is actually a rather old scientific issue now, since Lloyd and her sometimes collaborator, the late Stephen Jay Gould, have presented their arguments for many years. The basic issue is whether female orgasm itself has an adaptive purpose or whether it is merely a side effect of developmental processes that affect fetuses before sex differentiation occurs. Many potential adaptive purposes have been suggested, from the idea that females have orgasms more often with certain kinds of desirable mates, and therefore seek them out, to the idea that the contractions accompanying orgasm may create a suction effect to draw sperm further into the reproductive tract. The problem with any hypothesis is accounting for the fact that a large proportion of human sexual intercourse occurs without any female orgasm, and many females never experience orgasms.
To me, the Times article is interesting, and I recommend it for an overview. It doesn't follow standard journalistic protocol, but instead goes through a laundry list of different theories of the putative adaptive value of orgasm and Lloyd's objections to them. This makes for dry reading, but it does give a fair presentation of some of the alternatives (albeit with little detail). However, it leaves certain parts of Lloyd's argument unclear. For example, Lloyd indicates that
there was no doubt in her mind that the clitoris was an evolutionary adaptation, selected to create excitement, leading to sexual intercourse and then reproduction.
But if this is true, then what is the big deal about explaining female orgasm? Sure, it is possible that sexual arousal and excitement are adaptive while orgasm per se is not, but this seems increasingly like a distinction without a difference. And if female sexual excitement is adaptive, and if the nerve pathways are developmentally homologous between males and females, then why would anyone imagine that selection would necessarily cause the sexes to diverge in this aspect of their sexuality? Clearly one needs to read the book to find out the real story here.
Anyway, Gretchen tells me I have no business blogging about this because of my Y chromosomal status. And come to think of it, it is pretty twisted for Arianna Huffington to be touching all our lives this way....
Evolving allometry
Frankino AW, Zwaan BJ, Stern DL, and Brakefield PM. 2005. Natural selection and developmental constraints in the evolution of allometries. Science 307: 718-720. Science Online
On the subject of allometry between skeletal characters, there is a paper in the Februrary 4, 2005 Science that addresses the issue from the perspective of development. These researchers used an experimental population of butterflies to test the effect of natural selection on scaling relationships between body parts.
The paper begins by noting that body parts usually are scaled relatively tightly around a small range within species, but between species often show very different allometries with a higher range of variation. They considered two hypotheses to be likely explanations for this pattern. The first proposes that developmental constraints within species act to limit variability in scaling among characters. In this hypothesis, there are only certain ranges of sizes that can be taken on by any body part, because the development of that part is to some extent linked to the development of the rest of the body (or of some other part).
The second instead proposes that the variation within species is limited by natural selection underlying the scaling relationship. The hypothesis of selection would predict that some kinds of scaling relationships within a species are disadvantageous (to individuals) because they create a functional mismatch between the size of certain parts and the size of other parts or the whole.
The researchers in this study applied artificial selection to the area of butterfly forewings to study whether developmental constraits are underlying the allometry between this trait and body size. They found that the forewing area shared a strong genetic correlation (0.75) with pupal mass, and hypothesized that selection on forewing area should constrain the phenotypic evolution along the line of the intraspecific allometry.
They found that the forewing area responded rapidly to selection, without being accompanied by corresponding changes in body size. Although the allometry between these traits suggested that body size should change with selection on forewing area, it did not do so.
Our results, together with the few other studies that have used artificial selection to alter scaling relationships between morphological traits in insects, indicate that even strong genetic correlations do not constrain phenotype evolution in the short term. It seems that the developmental basis of these genetic correlations is more important than their strength in determining the response to selection. In particular, under novel selection regimes such as the artificial one we imposed, the developmental program coordinating the growth of the individual traits may influence how these traits and the relationship between them evolves (719).
After this selection, the researchers placed the altered populations in an open greenhouse environment and allowed them to compete with wild-type conspecifics. They assessed their reproductive success by examining marker powder transfer from males to females. They discovered that the wild-type males attained an average of three times as many matings as the males who had undergone selection on forewing area. "These results demonstrate strong stabilizing selection favoring the natural scaling relationship between forewing and body size in B. anynana" (719).
The researchers were not able to determine why males with the wild-type allometry had greater apparent mating success, although they present a number of hypotheses, including decreased locomotor performance, decreased ability to produce mating signals attractive to females, or decreased ability to compete with other males.
The overall conslusion is that the intraspecific allometry in these insects is primarily maintained not by developmental constraints, but instead by stabilizing selection acting on the allometry itself. In the face of strong genetic correlations between traits, the form of stabilizing selection on these allometries may result in
Gene flow and evolutionary dynamics::two bird studies
References:
Garant, Dany, Loeske E. B. Kruuk, Teddy A. Wilkin, Robin H. McCleery, and Ben C. Sheldon. 2005. "Evolution driven by differential dispersal within a wild bird population." Nature 433:60--65.
Postma, Erik and Arie J. van Noordwijk. 2005. "Gene flow maintains a large genetic difference in clutch size at a small spatial scale." Nature 433:65--68.
Here are two papers about evolution in field populations of wild birds, specifically great tits (Parus major). The first paper considers a single widespread population occupying a continuous woodland in England over 35 years. They measured nestling body mass, determined the genetic variance behind it, and discovered that the genetic variance is spatially variable among the eight sectors of the woodland. They found that this genetic variation among spatial locations is maintained by patterned dispersal. Specifically, smaller birds tended to migrate into a densely occupied habitat in the eastern part of the wood, while larger birds tended to migrate into the sparsely-occupied north. The authors speculate that larger birds were more successful in moving to more favored habitat where there is less mating competition. It is not known whether food availability or other ecological factors cause the difference in local population density, but the difference in mass in the migrating birds is not itself initiated by the new environment because the size differences are also reflected by their nestling mass in other parts of the wood. The interesting part of this study is that the authors were able to determine that birds with different genetic characteristics migrated to different places, and that differential dispersal partly causes the genetic differentiation of different subpopulations.
The second paper examines the clutch sizes of great tits on an island off the coast of the Netherlands. The island population is spatially structured, and the authors examined two subpopulations. While island birds tend to have smaller clutches, mainland birds have larger clutches. This difference is primarily due to genetic differences between island and mainland birds. The study observed the number of immigrant birds and their effects on the two island populations, which themselves differed significantly in clutch size. The interesting part of the study is that the authors were able to measure the fitness of birds with different clutch sizes, and thereby show that the level of selection in each of the island study populations was the same. Because the level of selection was the same, they can show that the difference in clutch size between the two island populations is entirely due to different levels of gene flow from the mainland.
Either of these studies may have interesting implications for human evolution. The idea that animals move in accordance with their physical characteristics is not entirely unexpected--since for example animals that tolerate cold better will be more likely to migrate to colder places. But the continuation of such genetically structured movement over substantial periods of time implies that genes may become spatially autocorrelated for adaptive reasons.
Why is this interesting? Think about Neandertals. They were clearly adapted differently from contemporary fossil humans, an adaptation that likely included different tolerance for cold, different energetic requirements and different habitat preferences. Traditionally, people have thought about these differences in terms of partial or complete reproductive isolation between Europeans and other populations. But an alternative is that the differences were maintained in the face of genetic contacts by structured dispersal. Consider that human hunter-gatherers live in small exogamous groups, with considerable contact with surrounding groups. In this circumstance, a dispersing individual may exercise substantial choice of new group, based on his or her (or others') knowledge. If there is a tendency toward assortative mating, or if individuals try to match their new group in some other way, then this population structure may induce the kind of structured dispersal that would maintain phenotypic gradients across space.
The second paper is less suggestive, but only because the joint effects of selection and gene flow have often been considered in thinking about the distribution of variation among ancient humans. Nevertheless, it is a good reminder that the effects of selection depend on the quantity of gene flow, and the effects of gene flow depend on the level of selection.
Evolution in demographic "sink" environments
Robert D. Holt and colleagues have published several papers recently concerning the evolutionary dynamics of populations in sink environments. These papers investigate a range of factors that might affect the degree of diversification and capacity for change of widespread animal species. I think they are very important as touchstones for understanding the past dynamics of human populations.
Within a metapopulation, a population sink is an area where the local environment does not allow reproduction at the replacement rate. Without an influx of migrants from other areas, the population within the sink habitat would eventually dwindle to nothing. Thus, the continued existence of a sink population depends on a long-term inflow of new individuals from other parts of the metapopulation.
In geographically structured metapopulations, it is very likely that some areas will be net population sinks, and others will be population sources, areas where the local population exceeds the replacement rate. A species will undoubtedly be more well adapted to some habitats than others. Among the subpopulations that belong to a species, reproduction will vary in accordance with local habitat quality. On evolutionary timescales, most species oscillate around a static population size. If the species as a whole reproduced substantially below replacement for a long time, it would become extinct. Thus, at any time we can predict that many of the subpopulations within a spatially-dispersed metapopulation will be population sources. As these source populations fill their local habitats to their maximum density, a natural response in species capable of dispersal is for individuals to move to lower-quality habitats. Garant and colleagues (2005) investigate the way that animals may direct their dispersal options to reflect local habitat quality and density-dependent competition.
Ultimately, many dispersing individuals will find themselves in local environments where the habitat quality is too low to support reproduction at the replacement rate. This is a population sink.
A population sink may be contrasted with a population that merely is too large for its local habitat to support. A population that has outgrown its habitat likely exhibits density-dependence, in which smaller population densities might have relatively high reproductive rates, but larger densities result in increased competition for resources and mates. With density-dependence, a growing population faces diminishing returns, as the rate of reproduction ultimately falls below replacement. The population may stabilize at an equilibrium size, or it may oscillate with alternating population crashes and expansions. In contrast, a population sink has no stable population size. Whether the population is small or large, it cannot sustain itself at its present size. The unique character of the sink is the necessity of repeated immigration to maintain the population.
Of course, over time the character of local environments and global climate may change, leading some areas to become more hospitable to a species and others to become less so. What this implies is that a particular area may be a population sink under one environmental regime, but that it may at a later point change--becoming a population source, a population reproducing at replacement, or an area where the species is locally extinct. Over long periods of time, some areas may be intermittent population sinks, meaning that they might exhibit inherent population growth (i.e. periods of positive growth) at some times, but other periods of time in which the population is sustained only by immigration. If the latter periods with negative reproductive rates are more significant over the long term, then the area may be termed a "net" population sink.
Center and edge
The population sink has clear relevance to the discussion of the center-and-edge effect. In terms of population dynamics, center-and-edge is a model of a simple metapopulation in which a major source population is geographically central, while the marginal populations reproduce at or under replacement rates. In this model, there is a stable gradient of gene flow from the center to the edge of the species' range, resulting from the presumed greater adaptation of the species to the central habitat and the compromised adaptation to the edge habitats. Smaller population sizes at the edges enable a greater rate of genetic drift. In the model, this creates a gradient of diversity, with the center population being more genetically diverse than edge populations.
Center-and-edge rests on the assertion that most species are best adapted to habitats in the center of their range. Or, playing to the possibility of a different geographic pattern, it metaphorically defines the center as whichever geographic area the population does exhibit the greatest adaptation to. So in the case of prehistoric humans, Africa is usually described as the population center--because it is where hominids originated, although it is clearly not at the center of the Pleistocene human geographic range.
But some of this confusion can be removed if a different metapopulation model is substituted, one in which Africa remained a source population during most of the Pleistocene, while East Asia and Europe remained net population sinks. The wild card here is South and West Asia, because the fossil evidence from these areas is so limited during most of the Pleistocene. It is clear that if Europe and East Asia were net population sinks, they must have been supported by immigrants originating in South Asia and West Asia, respectively. But were these regions themselves population sources or did they rely on immigrants ultimately from Africa? Without fossil evidence, this question can only be addressed with genetic comparisons of contemporary humans. These might be read as suggesting that West and South Asia were mainly conduits of migration between Africa and the more far-flung peripheries of Asia and Europe, but the evidence deserves a more comprehensive summary that might shed light on the matter.
So a metapopulation model that incorporates source and sink populations might describe the structure of the Pleistocene human population with greater accuracy than the center-and-edge account. But what does this transform? Plainly, if genetic drift was important to the establishment of regional human populations, it might equally work its effect in the more detailed metapopulation model as under the center-and-edge model. So the major advantage of center-and-edge, that it may explain the initial appearance of morphological differences among populations on the basis of a gradient of genetic diversity, is not lost.
But a fuller understanding of the force of selection on different populations is to be gained. These three papers on population sink dynamics are attempts to understand the evolution of niche breadth under the unique demographic context of a population that would naturally shrink without immigration from other places.
Allee effects in population sinks
Ecological specialization and population sinks
Local adaptation in population sinks
References:
@article{Holt:2004,
author = {Robert D. Holt and Michael Barfield and Richard Gomulkiewicz},
year = {2004},
title = {Temporal variation can facilitate niche evolution in harsh
sink environments},
journal = amnat,
volume = {164},
number = {2},
pages = {187--200} }
@article{Holt:Allee:2004,
author = {Robert D. Holt and Tiffany M. Knight and Michael Barfield},
year = {2004},
title = {{Allee} effects, immigration, and the evolution of species' niches},
journal = amnat,
volume = {163},
number = {2},
pages = {253--262} }
@article{Holt:2003,
author = {Robert D. Holt and Michael Barfield and Andrew Gonzalez},
year = {2003},
title = {Impacts of environmental variability in open populations
and communities: ``inflation'' in sink environments},
journal = theorpopbiol,
volume = {24},
pages = {315--330} }
Mitochondrial parasites
The story always is told that the symbiosis between early, free-ranging mitochondria and proto-eukaryotes was a virtual enslavement, with the eukaryotes consuming the mitochondria and making use of their energy-generation facility to the benefit of the eukaryotic cells.
Of course, the complete lack of free-ranging mitochondria and non-mitochondriated free-living eukaryotes today help to cast doubt on that account. Clearly the fate of both these ancestral organisms was to some extent sealed when they joined forces with each other.
Yet there is still the perception that the mitochondria somehow didn't gain as much as the eukaryotes. After all, almost all the genes of the mitochondria ended up being assimilated into the nuclear DNA. There is little left but a shadow of the original mtDNA. If the two could divorce, you have the sense that the nucleated cell would be much better off than its tiny organelle.
I wonder if it isn't equally plausible that the free-ranging mitochondria were parasites infecting eubacterial cells. The presumptive qualities of these proto-mitochondria would be really helpful for a parasite: they can pump out lots of ATP, which would be helpful in rapid infection and reproduction. Much of their DNA migrated readily into the nuclear DNA of eukaryotic cells, which would tend to support the idea that it was adapted to move outside the mitochondrion and manipulate host cell functions. And several kinds of non-eukaryotes appear to have remnant mitochondria-like organelles also (Emelyanov 2003, and citations therein).
This could also help to explain some other aspects of eukaryotic cells. For example, a nucleus and chromosome structure may both have originally protected host DNA from parasite manipulation. Differences in the tRNA population for mtDNA and nuclear genes may also stem from selection on parasitism.
I should mention that Emelyanov's 2003 paper also presents an interesting hypothesis for the origins of eukaryotes, and has much data from gene phylogenies to bring to bear. The idea is that the initial eukaryotes were chimeric with archaean and eubacterial elements, in an age when lateral gene transfer and merging of cells was more the rule. Could be.
References:
Emelyanov V. 2003. Mitochondrial connection to the origin of the eukaryotic cell. Eur J Biochem 270:1599. DOI link
Is this really news?
From a Reuters story:
Researchers at the University of Groningen in the Netherlands have used scans to show that different areas of the brain are stimulated during an orgasm but are not activated when a woman fakes it.
"Women can imitate orgasm quite well," Gert Holstege told a fertility meeting on Monday. "But there is nothing really happening in the brain."
Not exactly earth-shattering to anyone who's watched "When Harry Met Sally." But the story buries the lede:
But they did show that different parts of the male and female brain are activated and deactivated during sexual stimulation.
The researchers found less deactivation in the males in the areas of the brain linked to emotion and fear when they were sexually stimulated.
For more speculations about the mental features related to orgasm, see my previous post. Again, this is evidence that the feature itself cannot be disentangled from the cognitive features of the brain in humans. The article further says that in females, orgasm accompanies a deactivation of cortical regions and regions of the brain involved in fear and emotion.
On the other hand, these areas might naturally be less active in people willing to climax in a clinical setting while strapped into an MRI machine...
A convergent fossil panda's thumb
Stephen Jay Gould famously made the false thumb of the giant panda one of his hallmark examples of the structural vagaries of adaptation. His original essay, "The Panda's Peculiar Thumb" is available online, courtesy of the Unofficial SJG Archive.
Now, a PNAS paper by Manuel Salesa and colleagues reports evidence of a false thumb in a Miocene relative of the red panda:
The "false thumb" of pandas is a carpal bone, the radial sesamoid, which has been enlarged and functions as an opposable thumb. If the giant panda (Ailuropoda melanoleuca) and the red panda (Ailurus fulgens) are not closely related, their sharing of this adaptation implies a remarkable convergence. The discovery of previously unknown postcranial remains of a Miocene red panda relative, Simocyon batalleri, from the Spanish site of Batallones-1 (Madrid), now shows that this animal had a false thumb. The radial sesamoid of S. batalleri shows similarities with that of the red panda, which supports a sister-group relationship and indicates independent evolution in both pandas. The fossils from Batallones-1 reveal S. batalleri as a puma-sized, semiarboreal carnivore with a moderately hypercarnivore diet. These data suggest that the false thumbs of S. batalleri and Ailurus fulgens were probably inherited from a primitive member of the red panda family (Ailuridae), which lacked the red panda's specializations for herbivory but shared its arboreal adaptations. Thus, it seems that, whereas the false thumb of the giant panda probably evolved for manipulating bamboo, the false thumbs of the red panda and of S. batalleri more likely evolved as an aid for arboreal locomotion, with the red panda secondarily developing its ability for item manipulation and thus producing one of the most dramatic cases of convergence among vertebrates.
So not only is there the bamboo grasping story, there is also the climbing carnivore story. Incidentally, red pandas are much cuter than giant pandas, and they hardly get any attention at all.
The noble red panda
UPDATE (1/6/06): I just saw that Carl Zimmer blogged this story long before I did. It's a good story.
References:
Salesa MJ, Anton M, Peigne S, Morales J. 2006. Evidence of a false thumb in a fossil carnivore clarifies the evolution of pandas. Proc Nat Acad Sci USA Online early access. Abstract
Rerunning the clock
Stephen Jay Gould (among many others) used to claim that life's history has been highly contingent on unlikely events. These events were so unique that they couldn't be predicted to happen -- they just did. The implication is that if the history of life were run again from the beginning, the end result would turn out completely different.
Now certainly at some level that must be true. The fact that any particular species ends up the way it is depends on the concordance of so many independent events that it just couldn't turn out the same way twice. Not to mention that many of those independent events are rare mutations that might easily failed to happen, or if they did happen, might easily have been eliminated by drift instead of becoming adaptive subsitutions. From this perspective, the appearance of any one species is due to the combined probability of many extremely rare events. Multiply all those tiny probabilities by each other, and you get the probability that life would have turned out the way it has.
But some people have argued that there are aspects of the history of life that have a good chance of happening on any Earthlike planet. After all, some important things have evolved independently many times, like flight. Large-scale generalizations like Cope's rule that supposedly apply across many different phyla hint that there may be common factors affecting the evolution of very divergent body plans and ecological adaptations. Put these things together, and you get the impression that a new instance of life on another planet like ours might evolve in broadly similar ways, even if the specifics would certainly be very different.
Possibly the most important question of this kind is whether intelligence would be likely or unlikely to evolve on suitable life-bearing planets. This "historical contingency" issue has been a prominent part of discussions about "Drake's equation", which gives a back-of-the-envelope list of factors important to the chance we will find intelligent life elsewhere in the galaxy.
Now, this paper by Geerat Vermeij addresses the question with evidence.
Many events in the history of life are thought to be singular, that is, without parallels, analogs, or homologs in time and space. These claims imply that history is profoundly contingent in that independent origins of life in the universe will spawn radically different histories. If, however, most innovations arose more than once on Earth, histories would be predictable and replicable at the scale of functional roles and directions of adaptive change. Times of origin of 23 purportedly unique evolutionary innovations are significantly more ancient than the times of first instantiation of 55 innovations that evolved more than once, implying that the early phases of life's history were less replicable than later phases or that the appearance of singularity results from information loss through time. Indirect support for information loss comes from the distribution of sizes of clades in which the same minor, geologically recent innovation has arisen multiple times. For three repeated molluscan innovations, 28-71% of instantiations are represented by clades of five or fewer species. Such small clades would be undetectable in the early history of life. Purportedly unique innovations either arose from the union and integration of previously independent components or belong to classes of functionally similar innovations. Claims of singularity are therefore not well supported by the available evidence. Details of initial conditions, evolutionary pathways, phenotypes, and timing are contingent, but important ecological, functional, and directional aspects of the history of life are replicable and predictable.
Those early-to-evolve unique things might for the most part be events that foreclose later development of the same things, by the way.
My intuition about this problem has been that some things -- if not inevitable -- were at least pretty likely. I don't think the hominid lineage is that exceptional; I expect that we just happen to be the first ones to have gotten here. There is a limit to the extent that intuition can be quantified, but studies like this one block out the possibilities.
References:
Vermeij GJ. 2006. Historical contingency and the purported uniqueness of evolutionary innovations. Proc Nat Acad Sci USA Abstract
Notes on "Darwinian agriculture"
R. Ford Denison's blog, "This Week in Evolution," has become a very interesting read since he began a couple of months ago. Denison recently attended a symposium titled, "Darwinian Agriculture: the evolutionary ecology of agricultural symbiosis." He summarizes the basic idea of "Darwinian agriculture" in his pre-meeting post:
"Darwinian Agriculture: when can humans find solutions beyond the reach of natural selection?" was the title of a paper that Toby Kiers, Stuart West, and I published in 2003. Our answers to the title question suggested how increased understanding of past and ongoing evolution could improve: 1) breeding of crops and livestock, and 2) design of agricultural ecosystems.
With respect to genetic improvement of crop plants, we wrote:
"most simple, tradeoff-free options to increase competitiveness (e.g., increased gene expression, or minor modifications of existing plant genes) have already been tested by natural selection. Further genetic improvement of crop yield potential over the next decade will mainly involve tradeoffs, either between fitness in past versus present environments, or between individual competitiveness and the collective performance of plant communities."
Since then, every time I give a talk on this subject, I look for papers that might disprove this tradeoff hypothesis. I also look for examples of tradeoffs that were rejected by natural selection, but which might be acceptable in agriculture. For example, many people are working on improving drought tolerance of crops. Is it possible to improve on natural selection for this trait?
In other words, the concept is something like the agricultural version of evolutionary medicine. The past is important to the present, and understanding how crop plants were selected in past environments (both natural and agricultural) helps us to predict the likely constraints on their current adaptive potential. Further, those constraints might be relaxed by trading off some traits that in the past may have been strongly selected, but at present are of less adaptive importance.
Few people working to unravel evolutionary history stop to think about the practical implications of this research. And unfortunately, few people working in applied fields like agriculture or medicine think much about how knowledge about evolutionary history can be applied to modern problems. But this is changing -- more and more, it has become clear not only that the present is a product of the past, but also that the past helps to determine the future.
A second post was a follow-up to the symposium, reviewing some of the papers presented. A couple of papers on genetic diversity in modern cattle and their relationships to European aurochsen are reviewed. These are very interesting, and of course Greg Cochran and I wrote a short review of this story in our introgression paper last year.
Denison's quick review of his own presentation is a good illustration of conflicting selection in crop evolution, and attempts to reduce counterselection:
Finally, I talked about breeding crops that yield more per acre (or hectare) because individual plants compete less with each other. The best-known example is plant height. Short plants make more grain because they waste less on stems. This works well if you have a whole field of short plants. But, in a mixture, the taller, low-yield plants shade out the shorter high-yield plants. Plants that branch less can yield more, in monoculture, but can't compete against plants that branch more.
In this way, the unique practices that have helped to make agriculture such a productive system for humans can actually impede further response to selection -- as genetic variation within crop plants can include strategies that defy attempts to select for a given trait. It's game theory applied to corn! More to the point, selecting for short plants is an inefficient way to deal with the problem. Hybrids (and cloning) work as farming techniques not only because of overdominance, but also because making sure that your entire field is genetically uniform is a way of reducing the strategy options available to the plants.
One of the papers also covered the ecology of a non-human agricultural analogue: ant fungus farming:
In ant gardens, contact between two different fungal strains triggers a negative reaction that reduces growth. Even manure from ants that ate one strain will trigger this reaction in a second strain. In termite gardens, different fungal strains don't fight. But they don't bond, either, and this also limits growth. Over tens of millions of years, ants and termites have evolved behaviors that maintain their gardens as fungal monocultures. Ants remove alien fungi, even strains that might be grown by another ant colony. Termites prevent their fungi from reproducing sexually, by eating fruiting bodies that could produce sexual spores. Without sex, one strain gradually takes over.
Now that's what you call selective breeding. Of course, they have the same aim as humans. The best way to maximize the energy return of the fungus is to eliminate the possibility that it can disperse without your help! If you don't want your domesticate to lose productivity to cheater strategies (which attempt to disperse on their own), then you had better cut off all possibility of gene flow into your fungus garden.
Denison points out at the end of his post that this farming strategy itself is not always optimal:
Whether we look at ant or termite fungus gardens, microbes that help crops, or crops themselves, diversity can lead to interactions that reduce growth. Should we work to reduce diversity in agriculture, then? Not exactly. Diversity may be useful at some scales, but harmful at others. If the world grew more different crops, a disease that killed any one crop would have less effect. But that may not mean that every field should contain more than one crop.
Some of this confirms common sense -- Denison mentions crop rotation as a long-employed diversity management technique. But the details of the interactions of plant ecology, human management practices, and genetic correlations among different traits will be central to the future of agricultural science. It's a clear example of the practical importance of evolutionary theory.
Related posts here:
Roundup ready, a review of glyphosate resistance linking to a story on the emergence of coca plants resistant to Drug War-related herbicides.
More on bison and introgression, a post covering attempts to breed cattle genes out of bison, and vice versa.
The inevitability of introgression, covers my paper with Cochran.
Breeding nutritional Neanderwheat, on the introduction of genes from wild wheat relatives into domesticated wheat.
The island rule
Mark Lomolino has been one of the central figures in recent work on body size, energetics, and evolution -- especially with respect to the evolution of body size in island species. With several of his colleagues, he had an editorial in the Journal of Biogeography last year, calling for a renewed research agenda in ecogeographical rules -- that is, rules relating body size and other characters to biogeographic variation of different kinds. The island rule is one such rule, other examples are Bergmann's and Allen's rules (relating body size and limb lengths with temperature) and Rapoport's rule (relating north-south species range extents with actual latitude).
Most of the possibility for a substantial renewal has come from the increased exchange and computerized search capacity for basic observations on body size and shape in different species. The editorial mainly reviews the prospects for developing new theoretical understandings of these rules and their exceptions using new data, and points to the necessity of the comparative approach.
The editorial treats the island rule as a case study -- and it is probably the best one possible because of the substantial density of recent research on the topic. The authors provide a nice nutshell history of the development of the island rule as a scientific explanation:
Here we first summarize the epistemology of the island rule as an illustrative case study. This pattern was first described by Foster (1963, 1964), but it was not labelled as a rule (and one 'with fewer exceptions than any other ecotypic rule in animals') until Van Valen's papers in 1973 (Van Valen, 1973a,b: p. 35). Originally, Foster described the pattern as a tendency for different taxa (orders of mammals) to exhibit different evolutionary trends on islands, rodents tending to increase, and carnivores and ungulates tending to decrease in body size. Later, Heaney (1978), Lomolino (1985) and others reinterpreted the rule to be a graded trend from gigantism in the smaller species to dwarfism in the larger species of mammals. This recasting of the island rule reflected the heuristic tension between process and pattern, and theory and empiricism. The earliest articulation of the island rule suggested disparate evolutionary trends among mammalian orders, but this was soon found to be inconsistent with modern evolutionary theory. Rather than invoking some overriding importance of phylogenetic inertia that somehow differs among mammalian orders, the island rule (sensu nova) instead is inferred to reflect differences in selective pressures on islands and among species of different body size (therefore the graded trend should occur within, as well as among, mammalian orders; see explanations by Heaney, 1978; Lomolino, 1985, 2005; Adler & Levins, 1994; Adler, 1996; Marquet & Taper, 1998; McNab, 2001, 2002; Gould & MacFadden, 2004). Note, however, that the geographical context of the island rule's primary pattern is typically limited and binary: terrestrial populations occur in just two types of ecosystem, islands or mainland sites. Yet we know that islands vary in area, isolation, latitude and other characteristics that influence the abilities of organisms to colonize and maintain populations. Thus, in addition to the primary pattern, body size of insular populations of particular species should not be constant, but should vary in a non-random manner among islands and archipelagoes. These secondary or corollary patterns provide excellent opportunities to evaluate alternative explanations for the island rule, for example by testing for correlations between body size and the area, isolation and latitude of islands (see studies summarized in Table 3 of Lomolino, 2005), or equivalently by testing for dynamics in body size following range expansion and vicariance, or tectonic events, climatic fluxes and associated changes in productivity, community structure and isolation of habitats and populations (Case, 1976, 1982, 2002).
The editorial quickly details some of the current range of hypotheses addressing body size evolution in island contexts, and has a great set of references. I like this paragraph a great deal, it makes many suggestions for research strategies:
Perhaps most insightful among these new, more integrative research initiatives are the opportunities afforded by the many thousands of introduction 'experiments' performed by human civilizations during their advances across the globe. Each of these episodes of invasion provides an opportunity to investigate how the dynamics in one of the most fundamental characteristics of an organism - its body size - is associated with the dynamics in one of the most fundamental characteristics of a species - its geographical range. A limited, but intriguing number of studies have demonstrated that ecogeographical patterns can evolve in surprisingly short periods of time as an invasive species expands its exotic range and, as a result, experiences repeated founder events and novel selection regimes (Johnston & Selander, 1964; Huey et al., 2000, 2005; Gilchrist et al., 2001; Sax, 2001; Campbell & Echternacht, 2003; Fridley et al., 2006; Patterson et al., 2006). The converse phenomenon - changes in body size and other characteristics of individuals as the species' geographical range contracts - may prove just as insightful. We know that geographical range collapse is far from a random process, with final populations typically persisting in the most isolated reaches of the species' historical range, either along the range periphery, in montane areas or on oceanic islands (Lomolino & Channell, 1995; Channell & Lomolino, 2000a,b; see also Safriel et al., 1994; Towns & Daugherty, 1994; Gaston, 2003; Laliberte & Ripple, 2004). Yet we know of no studies examining the consequences of this highly non-random pattern of range collapse on body-size variation in native or invasive species (Lomolino et al. 2006:1505).
An integrative perspective on population ecology, adaptations, and displacement in the face of demographic change would certainly improve our understanding of human evolution. In particular, the events of the Late Pleistocene may be explicable only in these terms. But also, taking a broader view of ecological change, ecogeographical changes in Holocene human populations may be examined with this perspective.
In their list of suggestions, Lomolino and colleagues include this:
We should capitalize on the thousands of unplanned but well chronicled introduction 'experiments' as opportunities to investigate simultaneously the dynamics of morphological traits and geographical range size. Among these, we include the many waves of invasions and subsequent ecological and evolutionary adaptations of Homo sapiens. Given the available global record on colonization by human civilizations and the substantial morphological variation among individuals and regional populations, ecogeographical studies of our own species may prove especially intriguing (Roberts, 1953, 1978; Ruff, 1994; Bindon & Baker, 1997; Brown et al., 2004; Morwood et al., 2004) (Lomolino et al. 2006:1507).
Lately, with the exception of Flores, research into hominid body mass has emphasized global patterns rather than regional ones. But the most interesting questions lately have arisen as a result of observing interregional and within-region diversity in body sizes (particularly at the Australopithecus-Homo transition).
My favorite factoid lately -- you can ask my classes -- is the location of the tallest contemporary human population. The Netherlands.
References:
Lomolino MV, Sax DF, Riddle BR, Brown JH. 2006. The island rule and a research agenda for studying ecogeographical patterns. Journal of Biogeography 33:1503-1510. doi:10.1111/j.1365-2699.2006.01593.x
The incredible nonshrinking carnivores
The "island rule" is the prediction that small bodied animals should evolve larger sizes on islands, while large bodied animals should evolve to be smaller. Carnivores include a large range of sizes, from the "small" species that are supposed to evolve larger body sizes on islands, up to the "big" species that are supposed to shrink. Shai Meiri et al. (2005) studied the body sizes of carnivore faunas on islands compared to the sizes and degree of isolation of the islands, to see if they followed these predicted patterns.
They don't.
Why neutrally buoyant isn't weightless
Although fish are neutrally buoyant, they still have to push water out of the way to move forward, he said. That water raises the surface -- a phenomenon that is often imperceptible as it may be spread across an entire lake, stream or ocean.
"The water can only go up because the bottom and sides of the channel are rigid," Bejan said. "That bulge, however undetectable, is the fish's footprint."
Fish must, therefore, work against gravity to lift an amount of water equal to their own mass for each body length they move forward.
"It puts fish in the same physical realm as runners and fliers."
That's from an article about similarities in locomotor dynamics across swimmers, runners, and flyers. A bunch of engineers showed that common physical principles explain relationships between body mass and speed, stride (or wingbeat) frequency, and muscle force.
On the other hand:
"From simple physics, based only on gravity, density and mass, you can explain within an order of magnitude many features of flying, swimming and running," added James Marden, professor of biology at Penn State. "It doesn't matter whether the animal has eight legs, four legs, two, even if it swims with no legs."
I'm fairly sure that my own running speed is within an order of magnitude of almost everything with legs, regardless of its size. So a lot of biological interest is cruising beneath the radar of physical constraints. But these relations may explain why some mouse-elephant type allometries are relatively similar between fish, mammals, and birds.
UPDATE (1/2/06): A reader e-mails: "Am I missing something? Sure fish have to push water out of the way as they move forward, but that water has a perfectly good place to go: into the space the fish just vacated! There might be some small vertical displacement of water, but it's an entirely local phenomenon that has no effect on the surface."
That seems like a good point to me. You might as well say that cars have to push air uphill in order to move forward (albeit with much less mass). Hmmm....
The shrinking sloths of Panama
Anderson and Handley (2002) presented an analysis of the evolution of three-toed sloths on the islands of Bocas del Toro, Panama. These islands were part of the mainland during the last glaciation, and became isolated by rising sea levels during the past 10,000 years. Some of the islands remained connected to the mainland, and to each other, for longer than others. On each of five islands, the living sloths are much smaller than the average size of sloths on the mainland. On one of the islands, this size reduction is so great (seven standard deviations) that Anderson and Handley (2001) suggested that the island population be assigned to a new species.
The example is the closest to a controlled experiment in island dwarfing that we are likely to find. The time that each island was isolated has been well established based on ancient sea levels and the ages of depth-sensitive corals between them. All of the islands have the same ecology, with the exception of species lost after the islands were isolated. The sloths are represented by subfossil deposits as well, which provide samples of their evolution over time.
Hence, it is a very important example for testing mechanisms and patterns of evolution when continental species are isolated on islands. The paper includes many valuable brief reviews of issues related to evolution in this context. I'm finding this paper tremendously useful to me right now, so I'm taking a number of notes and also including some of the bibliographic references. Several of these are references I've used before, but this is a convenient topic to gather together some references on evolutionary rates as well as biogeography.
Is a new method going to "shake up" hominid phylogenetics?
No.
Oh, you know I can't manage a one-word post here. I can't get the paper yet -- now Nature has moved to the annoying press-release-long-before-paper-appears model! But I haven't read anything in the press yet that makes any sense. Most stories (and here) just seem to be press-release-regurges.
To me, this is the key passage:
The team goes back over the same well-known set of specimens, but uses a different approach to analyse it, focussing in particular on a set of fundamental yet long-term changes in skull shape.
They took digital 3D images of the casts of 17 hominid specimens as well as from a gorilla, chimpanzee and H. sapiens.
Well, that certainly sounds like the way we teach 100-level hominid phylogeny labs when we only have 17 casts. But it doesn't sound very much like the kind of careful character analysis that ought to go into a test of a phylogenetic hypothesis.
UPDATE(2008/05/06): More thoughts upon reading the paper here.
"Spacecraft all over the Pliocene"
Rex Dalton has a great two-page article in Nature about the bush vs. ladder dispute. It keys off of the Middle Awash Australopithecus anamensis article by White and colleagues from a couple of weeks ago.
If you recall that one, White et al. posited that Ardipithecus was likely ancestral to Au. anamensis, and that the two did not overlap in time. Here's the key exchange in the Dalton piece:
This month's Nature paper makes a bold argument, and shows the Awash team seeking to put its mark on the record. Others in the
field are impressed. "When you find 30 new hominid fossils, you are allowed a certain amount of conjecture," says Bernard Wood, a palaeoanthropologist at George Washington University in Washington DC. "As always, they have done a fantastic job."
But he and others are unconvinced by the Awash team's conclusion: "This is only the first half of the rugby match," says Wood. Meave Leakey, lead author on the Au. anamensis discoveries in Kenya, is more blunt. "I don't believe this," she says. "We do not have the specimens to fill the gaps."
Leakey and Wood are among those who believe that other, as yet undiscovered hominid species may have lived at this time, from 4.4 million to 2.9 million years ago. The existence of other species would cloud or eliminate the argument for a direct lineage. "My prejudice is there are more lineages rather than fewer -- more diversity," says Wood. "I have to concede these new data are dramatic. But we should beware coming out with a complete explanation when we don't have all the
evidence."
This argument frustrates White. "There were Martians there back then too," he says. "And spacecraft all over the Pliocene -- we just haven't found them yet."
Waiting for Monte Cassino
In a series of articles since 2000, White and colleagues have laid out a systematic attack on the "bushy" phylogeny model. Their arguments have extended across four million years and seven species, with a breadth that rivals the Allies breaking the Winter Line.
Consider the angles of attack:
1. Au. anamensis -- Au. afarensis. Everyone basically accepts that Au. anamensis is a direct ancestor of Au. afarensis. And the two species are really not very different from each other -- for instance, they are more alike than either is to Ardipithecus. The transition between these species would look to be a simple case of anagenesis, except......for Kenyanthropus (Leakey et al. 2001). This small-toothed, flat faced hominid needs an ancestor, too. Au. anamensis might have been the common ancestor of Kenyanthropus and Au. afarensis. If so, then both these later species originated by cladogenesis from Au. anamensis. A similar argument might be made for other species, like Australopithecus bahrelghazali (Brunet et al. 1996) or the Sterkfontein Member 2 hominids. But Au. bahrelghazali is only known from a partial mandible and only differs from Au. afarensis by a three-rooted premolar, which is considered by many to be weak evidence, and the Sterkfontein Member 2 sample has not yet been taxonomically assigned -- they might turn out to be Au. afarensis, for example. Kenyanthropus remains the strongest case for cladogenesis (i.e., a "bush"). Yet...
...White (2003) denied that the Lomekwi skull KNM-WT 40000 was a distinct species. In particular, he argued that the extensive postmortem deformation of the skull made it impossible to substantiate an anatomical difference from Au. afarensis, and even if it was different, the anatomical diversity of living hominoid species is so great that it would probably encompass the difference between KNM-WT 40000 and known Au. afarensis crania.
2. Earliest hominids. At the moment, the earliest putative hominids include three genera: Orrorin (Senut et al. 2000), Sahelanthropus (Brunet et al. 2002), and Ardipithecus, represented in the Late Miocene by Ar. kadabba (Haile-Selassie 2001, Haile-Selassie et al. 2004). Evidence for obligate bipedality has been challenged (by different researchers) for each of these three (I'm one of those who has questioned bipedality for Sahelanthropus).So far the only comparable anatomical parts from all three samples are teeth...
...which were examined by Haile-Selassie, Suwa and White (2004). They concluded that the variation among these three genera
is no greater in degree than that seen within extant ape genera. Despite claims of molar enamel thickness differences among these late Miocene fossils, we question the interpretation that these taxa represent three separate genera or even lineages. Given the limited data currently available, it is possible that all of these remains represent specific or subspecific variation within a single genus (Haile-Selassie et al. 2004:1505).
Additionally, Ohman, Lovejoy and White (2005) challenged the interpretation of the internal anatomy of the Orrorin femur, which had been suggested to be more derived than that of Au. afarensis. They wrote:
We agree that the Lukeino femur's external morphology suggests some form of bipedality. Yet the more detailed original scans appear to show a distinct superior cortex different from Australopithecus and humans, with the cortex distribution being more primitive than that seen in any other hominid, including Australopithecus.
The relevance of this argument to the phylogenetic diversity of early hominids depends on the anatomy of the Ardipithecus femur, which none of the rest of us are in a position to know. But one may speculate that if all these early "hominids" had femora with similar morphology, it would further reinforce the interpretation that they belong to a single lineage.
3. Ardipithecus -- Au. anamensis. This is the current example. Here's how Dalton discusses it:The latest Afar discovery is exciting experts because it shows that the three hominids existing in the same area, but in successive time periods. Tim White of the University of California, Berkeley, co-leader of the Awash team, believes this points to a direct lineage between the three -- a process called phyletic evolution. The new Au. anamensis fossils are only 300,000 years younger than Ar. ramidus, meaning that if one became the other, the changes would have had to happen that fast. But the key point, says White, is that fossils of Au. anamensis and Au. afarensis have never been found in sediments the same age as those containing Ar. ramidus. If fossils of the different species were found together, that could show that they belonged to multiple lineages existing simultaneously.
Finding remains of all three species in the same area but not from the same time period suggests they did not coexist, says White.
...
The specimens also provide anatomical clues to evolutionary history. "The new Au. anamensis fossils are anatomically intermediate between the earlier Ar. ramidus and the later Au. afarensis," says White. For example, the teeth of the newly discovered Au. anamensis fossils seem adapted to chew tougher and more abrasive foods than Ar. ramidus. The researchers believe this shows that Au. anamensis had a broader diet. "All this strengthens the view that there is phyletic evolution from Ar. ramidus through Au. anamensis," says White. He believes he has nailed down the relationship between the two later species, although he says that further specimens are needed to prove the earlier link (Dalton 2006:1100).
Of course, it would help matters if we knew in more detail what Ardipithecus looked like. But one must imagine that the stage is being set for its revelation. The unilineal interpretation places Ardipithecus at the critical point as an ancestor to the major mid-Pliocene australopithecine lineage. Extending the unilineal interpretation earlier into the Late Miocene would make Ardipithecus the earliest hominid as well.
It is not necessary to think that taxonomic uniformity means anatomical uniformity, though. Ardipithecus already encompasses a trend of decreasing canine size and less sectorial P3 for example. A trend toward fuller skeletal adaptation to bipedality may also be imagined. But in that context, it is important to note that the time interval between the Orrorin femur and the unpublished Aramis skeleton is longer than the time between Aramis and Hadar. Those relative times may become quite important in thinking about the evolution of those postcrania.
The Winter Line was broken at Monte Cassino, after many failed attempts from different approaches. The Aramis fossils are either the heavy shoe waiting to drop, or they are the uncomfortable foot that all this talk about phyletic evolution is meant to shoehorn into place.
Commentary
If all these cases are added together, they imply a single evolving lineage encompassing at least four anagenetic taxa, Ar. kadabba -- Ar. ramidus -- Au. anamensis -- Au. afarensis. This last would presumably be followed by a cladogenesis into a robust australopithecine species (Australopithecus aethiopicus) and Australopithecus africanus.
One could add Homo erectus to this list, since White and colleagues argued in their description of the Daka skull (Asfaw et al. 2002) that the Asian and African samples represent one cosmopolitan species.
But then one species sticks out as a surprising exception to the pattern: Australopithecus garhi (Asfaw et al. 1999). It will be interesting to see a close argument showing why this species is really different from South African Au. africanus. Say, more different than KNM-WT 40000 is from the Hadar crania. It's quite glaring, really, that this species should be there mucking up such a simple phylogeny.
I have to say, after reviewing all these papers in one sitting -- this entire bush vs. ladder thing is getting very tiresome! I mean, isn't there something else that we could organize early hominid discoveries by? These are all papers in the top journals, and this is the (fairly specialized) discussion that has been promoted as the central issue in the field!
The subtitle of the Dalton piece suggests that it is merely a philosophical difference:
Deciding whether our ancestors evolved as a single lineage may depend more on philosophy than fossils.
But that's not really true. There is a clear null hypothesis here, quite directly drawn from William of Ockham:
entia non sunt multiplicanda praeter necessitatem
Which of course means:
Sometimes fossil samples really do form ancestor-descendant relationships.*
(*) It doesn't really. It means "Entities should not be multiplied beyond necessity."
References:
Asfaw B, Gilbert WH, Beyene Y, Hart WK, Renne PR, WoldeGabriel G, Vrba ES, White TD. 2002. Remains of Homo erectus from Bouri, Middle Awash, Ethiopia. Nature 416:317-320. DOI link
Asfaw B, White T, Lovejoy O, Latimer B, Simpson S, Suwa G. 1999. Australopithecus garhi: A new species of early hominid from Ethiopia. Science 284:629-635. DOI link
Begun DR. 2004. The earliest hominins -- is less more? Science 202:1478-1480. DOI link
Brunet M. and 37 others. 2002. A new hominid from the Upper Miocene of Chad, Central Africa. Nature 418:145-151. DOI link
Brunet M, Beauvillain A, Coppens Y, Heintz E, Moutaye AHE, Pilbeam D. 1995. The first australopithecine 2,500 kilometres west of the Rift Valley (Chad). Nature 378:273-275. DOI link
Dalton R. 2006. Feel it in your bones. Nature 440:1100-1101. DOI link
Haile-Selassie Y. 2001. Late Miocene hominids from the Middle Awash, Ethiopia. Nature 412:178-181. DOI link
Haile-Selassie Y, Suwa G, White TD. 2004. Late Miocene teeth from Middle Awash, Ethiopia, and early hominid dental evolution. Science 303:1503-1505. DOI link
Leakey MG, Spoor F, Brown FH, Gathogo PN, Kiarie C, Leakey LN, McDougall I. 2001. New hominin genus from eastern Africa shows diverse middle Pliocene lineages. Nature 410:433-440. DOI link
Ohman JC, Lovejoy CO, White TD. 2005. Questions about the Orrorin femur. Science 307:845. DOI link
Senut B, Pickford M, Gommery D, Mein P, Cheboi K, Coppens Y. 2001. First hominid from the Miocene (Lukeino formation, Kenya). Comptes Rendus 332:137-144.
White T. 2003. Early hominids -- diversity or distortion? Science 299:1994-1996. DOI link
Criticizing the genetic variance-covariance matrix
A subset of evolutionary theorists are specifically concerned with how the evolution of multiple characters of organisms are linked to each other by genetic correlations. A handful of those theorists actually think about human evolution. There is a little bit of matrix algebra involved; ma