Razib Khan One-stop-shopping for all of my content

June 20, 2011

Convergent evolution happens!

In the image to the left you see three human males. You can generate three pairings of these individuals. When comparing these pairs which would you presume are more closely related than the other pairs? Now let me give you some more information. The rightmost image is of the president of Tanzania. The middle image is of the president of Taiwan (Republic of China). And finally, the leftmost image is of the prime minister of Papua New Guinea. With this information you should now know with certainty that the prime minister of Papua New Guinea and the president of Taiwan are much more closely related than either are to the president of Tanzania. But some of you may not have guessed that initially. Why? I suspect that physical inspection may have misled you. One of the most salient visible human characteristics is of the complexion of our largest organ, the skin. Its prominence naturally leads many to mistakenly infer relationships where they do not exist.

This was certainly an issue when European explorers encountered the peoples of Melanesia. An older ...

November 24, 2010

The inevitable social brain

ResearchBlogging.orgOne of the most persistent debates about the process of evolution is whether it exhibits directionality or inevitability. This is not limited to a biological context; Marxist thinkers long promoted a model of long-term social determinism whereby human groups progressed through a sequence of modes of production. Such an assumption is not limited to Marxists. William H. McNeill observes the trend toward greater complexity and robusticity of civilization in The Human Web, while Ray Huang documents the same on a smaller scale in China: A Macrohistory. A superficial familiarity with the dynastic cycles which recurred over the history of Imperial China immediately yields the observation that the interregnums between distinct Mandates of Heaven became progressively less chaotic and lengthy. But set against this larger trend are the small cycles of rise and fall and rise. Consider the complexity and economies of scale of the late Roman Empire, whose crash in material terms is copiously documented in The Fall of Rome: And the End of Civilization. It is arguable that it took nearly eight centuries for European civilization to match the vigor and sophistication of the Roman Empire after its collapse as a unitary entity in the 5th century (though some claim that Europeans did not match Roman civilization until the early modern period, after the Renaissance).

It is natural and unsurprising that the same sort of disputes which have plagued the scholarship of human history are also endemic to a historical science like evolutionary biology. Stephen Jay Gould famously asserted that evolutionary outcomes are highly contingent. Richard Dawkins disagrees. Here is a passage from The Ancestor’s Tale:

…I have long wondered whether the hectoring orthodoxy of contingency might have gone too far. My review of Gould’s Full House (reprinted in A Devil’s Chaplain) defended the popular notion of progress in evolution: not progress towards humanity – Darwin forend! – but progress in directions that are at least predictable enough to justify the word. As I shall argue in a moment, the cumulative build-up of compelx adaptations like eyes strongly suggest a version of progress – especially when coupled in imagination with of the wonderful products of convergent evolution.

Credit: Luke Jostins
Credit: Luke Jostins

One of those wonderful products is the large and complex brains of animals. Large brains are found in a disparate range of taxa. Among the vertebrates both mammals and birds have relatively large brains. Among the invertebrates the octopus, squid and cuttlefish are rather brainy. The figure to the right is from Luke Jostins, and illustrates the loess curve of best fit with a scatter plot of brain size by time for a large number of fossils. The data set is constrained to hominins, humans and their ancestors. As you can see there is a general trend toward increase cranial capacities across all the human populations. Neandertals famously were large-brained, but they exhibited the same secular increase in cranial capacity as African Homo. On the scale of Pleistocene Homo and their brains the idea of the supreme importance of contingency seems ludicrous. Some common factor was driving the encephalization of humans and their near relations over the past two million years. This strikes me as very strange, as the brain is metabolically expensive, and there are plenty of species with barely a brain which are highly successful. H. floresiensis may be a human instance of this truism.

But what about the larger macroevolutionary pattern? Is there a trend toward larger brain sizes in general, of which primates, and humans in particular, are just the most extreme manifestation? Some natural historians have argued that there is such a trend. But, there is a question as to whether increased brain size is simply a function of allometry, the pattern where different body parts and organs tend to correlate together in size, but also shift in ratio with scale. The nature of physics means that very large organisms have to be more robust because their mass increases far faster than their surface area. By taking the aggregate relationship between body size and brain size, and examining the species which deviate above or below the trend line, one can generate an encephalization quotient. Humans, for example, have a brain which is inordinately large for our body size.

And yet there are immediate problems looking at relationships between body and brain size, and inferring expectations. Different species and taxa are not interchangeable in very fundamental ways, and so a summary statistic or trend may obscure many fine-grained details. A new paper in PNAS focuses specifically on various mammalian taxa, corrects for phylogenetics, and also relates encephalization quotient by taxa to the proportion of social animals within each taxon. Encephalization is not a universal macroevolutionary phenomenon in mammals but is associated with sociality:

Evolutionary encephalization, or increasing brain size relative to body size, is assumed to be a general phenomenon in mammals. However, despite extensive evidence for variation in both absolute and relative brain size in extant species, there have been no explicit tests of patterns of brain size change over evolutionary time. Instead, allometric relationships between brain size and body size have been used as a proxy for evolutionary change, despite the validity of this approach being widely questioned. Here we relate brain size to appearance time for 511 fossil and extant mammalian species to test for temporal changes in relative brain size over time. We show that there is wide variation across groups in encephalization slopes across groups and that encephalization is not universal in mammals. We also find that temporal changes in brain size are not associated with allometric relationships between brain and body size. Furthermore, encephalization trends are associated with sociality in extant species. These findings test a major underlying assumption about the pattern and process of mammalian brain evolution and highlight the role sociality may play in driving the evolution of large brains.

A key point is that the authors introduce time as an independent variable, so they are assessing encephalization over the history of the taxon. This is clearly relevant for humans, but may be so for other mammalian lineages. The table and figures below show the encephalization slope generated by using time and body size as the predictors and brain size as the dependent variable. A positive slope means that brain size is increasing over time.

Two major points:

- Note that the slope is sensitive to the level of taxon one is examining. A closer focus tends to show more variance between taxa. So, for example, humans distort the value for primates in general. Bracketing out anthropoids paints a more extreme picture of encephalization, a higher slope. In contrast, the lemurs and their relatives exhibit less encephalization over time.

- The correlation between proportion of species which exhibit sociality and encephalization of the taxon is strong. From the text:

Encephalization slopes were correlated with both the proportion of species with stable groups (order R = 0.92, P = 0.005, n = 6; suborder R = 0.767, P = 0.008, n = 9; Fig. 2 A and B) and the proportion in either facultative or stable social groups (order R = 0.804, P = 0.027, n = 6; suborder R = 0.63, P = 0.04, n = 9).

The last figure makes it is clear that the correlations are high, so the specific values should not be surprising. Don’t believe these specific figures too much, how one arranges the data set or categorizes may have a large effect on the p-value. But the overall relationship seems robust.

266px-Alienigena
A highly encephalized “alien”

What to think of all of this? If you don’t know, one of the authors of the paper, Robin Dunbar, has been arguing for the prime importance of social structure in driving brain evolution among humans for nearly twenty years. The relationship is laid out in his book Grooming, Gossip, and the Evolution of Language. Robin Dunbar is also the originator of the eponymous Dunbar’s number, which argues that real human social groups bound together by interpersonal familiarity have an upper limit of 150-200. He argues that this number arises because of the computational limits of our “wetware,” our neocortex. Those limits presumably being a function of biophysical constraints.

One interesting fact though is that the median cranial capacity of our species seems to have peaked around one hundred thousand years ago. The average human today has a smaller brain than the average human alive during the Last Glacial Maximum! (see this old post from Panda’s Thumb, it’s evident in the charts) This may be simply due to smaller body sizes in general after the Ice Age. Or, it may be due to the possibility that social changes with the rise of agriculture required less brain power.

Ultimately if Dunbar and his colleagues are correct, if social structure is the most powerful variate in explaining differences in brain size when controlling for phylogenetics and body size, then in some ways it is surprising to me. After all, it does not seem that ants have particularly large brains, despite being extremely social and highly successful. Clearly the hymenoptera and other social insects operate on different principles from mammals. Instead of
developing “hive minds,” it seems as if in mammals greater social structure entails greater cognitive structure.

Citation: Susanne Shultz, & Robin Dunbar (2010). Encephalization is not a universal macroevolutionary phenomenon in mammals but is associated with sociality PNAS : 10.1073/pnas.1005246107

September 10, 2010

Leaping to a bigger brain

800px-RedRooYears ago an evolutionary biologist mentioned to me almost offhand that with the emergence of genomics and the necessity to master computational techniques a lot of the labor hours which may have gone into a more thorough understanding of specific organisms had gone by the wayside. He believed that his Ph.D. advisor was going to take a lot of knowledge with him when he retired because there was just no time to devote to discussing details of specific organismic life history, anatomy, and behavior. I obviously think that the sacrifice has been worth it, the new methods are powerful and answer long standing questions (or hold promise to do so), but something has no doubt been lost. Biological variation is such that a gestalt “big picture” sense of the lay of the land is useful. Much of biology is a historical science, and like history the details are of the essence. But unlike history biology is a natural science, and amenable to experimentation and observation, as well as laced with a more thorough formalization (yes, I am aware of cliometrics). The mileage one gets out of theory in biology is far greater than in history, as evidenced by the high prestige of an evolutionary framework, and the obscurity of cliodynamics (and the relative marginal reputation of Arnold Toynbee).

But evolution purely as logic often fails. The old debate between the balance & classical schools in evolutionary genetics was upended by empirical findings in molecular evolution in the 1960s, which subsequently stimulated neutral theory. Natural science has to extend itself through a long-term dance between system building and empirical verification or falsification. The seeds of new systems don’t come from a vacuum, rather, the prior set of observations and experiments lay the groundwork and serve as points of embarkation.

ResearchBlogging.orgThe combination of biology’s variation and its reliance on theories, heuristics, and rules-of-thumb (e.g., 19th century biology’s love affair with “laws”), often leads to perplexing surprises when a more systematic or deeper read of the data flies in the face of expectations. So it is with a new paper in PNAS which upends some specific relationships between mammalian characteristics and encephalization, as well as some more general prejudices. Brain size, life history, and metabolism at the marsupial/placental dichotomy:

The evolution of mammalian brain size is directly linked with the evolution of the brain’s unique structure and performance. Both maternal life history investment traits and basal metabolic rate (BMR) correlate with relative brain size, but current hypotheses regarding the details of these relationships are based largely on placental mammals. Using encephalization quotients, partial correlation analyses, and bivariate regressions relating brain size to maternal investment times and BMR, we provide a direct quantitative comparison of brain size evolution in marsupials and placentals, whose reproduction and metabolism differ extensively. Our results show that the misconception that marsupials are systematically smaller-brained than placentals is driven by the inclusion of one large-brained placental clade, Primates. Marsupial and placental brain size partial correlations differ in that marsupials lack a partial correlation of BMR with brain size. This contradicts hypotheses stating that the maintenance of relatively larger brains requires higher BMRs. We suggest that a positive BMR–brain size correlation is a placental trait related to the intimate physiological contact between mother and offspring during gestation. Marsupials instead achieve brain sizes comparable to placentals through extended lactation. Comparison with avian brain evolution suggests that placental brain size should be constrained due to placentals’ relative precociality, as has been hypothesized for precocial bird hatchlings. We propose that placentals circumvent this constraint because of their focus on gestation, as opposed to the marsupial emphasis on lactation. Marsupials represent a less constrained condition, demonstrating that hypotheses regarding placental brain size evolution cannot be generalized to all mammals.

The prejudice, which they mention in the text, is that marsupials are relatively small-brained vis-a-vis placentals. Though modern biology long ago rejected an explicit Great Chain of Being, I still think it is very hard to avoid the implicit working model that marsupials are somehow fundamentally inferior to placentals, and their stronghold in Australia and Melanesia is a manner of historical contingency (I believe this is an outgrowth of natural anthropocentrism). Additionally the authors claim that the fixation on kangaroos and their relatives as the exemplary marsupials has also given an improper impression of the clade’s encephalization. Similarly, the inclusion of primates distorts the overall perception of encephalization among placentals. The first figure makes clear as a descriptive matter the reason for our misimpression. I’ve reedited and labeled for clarity.

marsbrain1

Phylogenetic generalizations are naturally sensitive to the clades you are evaluating across. Prior to reading this paper my own understanding was that placentals were invariably larger-brained for their body size than marsupials. This is true still. But to a great extent this is simply an outcome of the placement within the placental clade of primates, a group which is atypical for mammals as a whole, placental or marsupial.

Next they looked at the log-transformed values of three traits against body mass in grams. I’ve rotated the figure, but you see panel A, B, and C, brain weight, BMR, and gestation + weaning age.

marsbrain2

Biological organisms are constrained to some extent by physical parameters, so all mammals follow roughly the same scaling trends. But, there are differences between placentals, marsupials, and monotremes. Interestingly smaller marsupials, those below 43 grams, are more encephalized than placentals of the same size. Placentals tend to have somewhat higher basal metabolic rates, BMR, than marsupials, and especially monotremes. Finally, the last figure shows a looser trend line with a larger residual. I suspect it’s because it is more about life history than a concretely physical parameter. In any case, here marsupials are above the placental trend line, in large part because marsupial young have a long phase of dependence on the mother after birth. In contrast placentals invest much more time and energy on gestation. This period is especially important for the question of encephalization, since so much of brain growth and development occurs during this early phase.

The third figure and the first table show the partial correlations between the traits of interest, and the regression slopes for the various traits in terms of their prediction of encephalization. I’ve reedited the figure and table a bit, including only the phylogenetically corrected regression. Filled arrows indicate positive correlations, and open arrows negative ones. The partial correlations are separate also for marsupials and placentals:

marsbrain3

A quick scan of the regression table shows that marsupials and placentals seem to show very different relationships between the predictors and encephalization. BMR is predictive of encephalization in placentals, and explains about ~10% of the variation (the r-squared). There is no statistically significant relationship in marsupials. Rather, ~20% of the variation in encephalization in marsupials is predicted by weaning age. Knowing what we know about marsupials, that they have relatively short gestations and long periods of dependence on maternal provisioning through lactation, this seems unsurprising. Weaning age is important in placentals, but less so. Rather, some of the “slack” seems to be taken up by gestation amongst them. Litter size is a strong negative predictor of encephalization. This seems to follow our intuition. There’s a trade off between quality and quantity of offspring.

It isn’t just placentals and marsupials that the authors contrast in this paper. They bring up another vertebrate lineage which has evolved toward relatively large brains and high basal metabolic rates: birds. Like marsupials the correlates of greater encehpalization among birds seems to be rather different from placentals. This is fundamentally a story of different strokes. Next I’d like to see cephalopods added to the equation! Rather than going into the details any further, let me jump to the conclusion:

Our results confirm several hypotheses of mammalian brain size evolution—in particular, the prediction of the maternal energy hypothesis that large-brained mammals with lower BMRs should have extended maternal investment times. In addition, our inclusion of marsupials provides further insight into the patterns of mammalian brain size evolution by showing that placental brain size evolution represents a unique case among mammals, connected with the placental reproductive emphasis on gestation. Based on this, several avenues for further research arise. If BMRs exceed brain maintenance rates in extant mammals, investigation of brain size in mammalian ancestors will provide clues as to when (and perhaps how often) the minimum BMR to allow a mammalian-sized brain evolved. Due to the close interaction between reproduction related brain size correlates and brain ontogeny, an improved understanding of brain growth and structural development patterns in species with different reproductive strategies emerges as another important area of future research. Our results emphasize that factors influencing the evolution of brain size are complex and emerge from fields that are traditionally researched separately, such as physiology, developmental biology, zoology, and paleontology. The integration of such interdisciplinary research represents the most appropriate avenue for providing a comprehensive evolutionary background for neurobiological research.

What if some of what you knew was wrong? To me if this paper checks out that’s going to be a take home for me. I simply assumed that placentals were highly encephalized in relation to marsupials. That seems not to be the case. Additionally, it seems that the trait level correlations of encephalization vary by phylogenetic clade, so that there are different ways to ascend the peaks of the big-brained. I take a deep interest for a very human reason, this figure generated by Luke Jostins:
linearThe figure shows the encephalization over time of various human lineages. In particular, it shows that disparate branches of the human family tree were all simultaneously increasing their cranial capacities until about ~200,000 years ago. Why? To understand, or at least generate some plausible explanations, we need to get a better grasp of encephalization across mammals, and further out across the animal kingdom. Recall that new systems emerge from previous patterns of observations. Primates are already the outliers among placental mammals, and we are the outliers among primates. Something very strange has been going on across our lineage for the past two million years, and we don’t quite know yet. Don’t tell Robert Wright, but I’m beginning to wonder if humanity was inevitable. At least after a certain point.

Citation: Weisbecker V, & Goswami A (2010). Brain size, life history, and metabolism at the marsupial/placental dichotomy. Proceedings of the National Academy of Sciences of the United States of America PMID: 20823252

Image Credit: Wikimedia

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