Snakes on the brain

Well, it hit Slashdot, so here goes:

Snakes as agents of evolutionary change in primate brains
Lynne A. Isbell

The abstract is really long. I'm going to quote all of it, but I'm separating into sections and adding numbers [in brackets] for further comment:

[1] Current hypotheses that use visually guided reaching and grasping to explain orbital convergence, visual specialization, and brain expansion in primates are open to question now that neurological evidence reveals no correlation between orbital convergence and the visual pathway in the brain that is associated with reaching and grasping. An alternative hypothesis proposed here posits that snakes were ultimately responsible for these defining primate characteristics.

In other words, you can reach and grasp with one eye closed. More below.

[2] Snakes have a long, shared evolutionary existence with crown-group placental mammals and were likely to have been their first predators.

Opportunity.

[3] Mammals are conservative in the structures of the brain that are involved in vigilance, fear, and learning and memory associated with fearful stimuli, e.g., predators. Some of these areas have expanded in primates and are more strongly connected to visual systems. However, primates vary in the extent of brain expansion. This variation is coincident with variation in evolutionary co-existence with the more recently evolved venomous snakes. Malagasy prosimians have never co-existed with venomous snakes, New World monkeys (platyrrhines) have had interrupted co-existence with venomous snakes, and Old World monkeys and apes (catarrhines) have had continuous co-existence with venomous snakes.

Not obvious that brain expansion and conservative fear pathways are really related to each other. Since there are many interconnections between different brain regions, it is not at all persuasive that some of the brain areas connected to fear response and learning are connected to neocortical areas that evolved within primates.

[4] The koniocellular visual pathway, arising from the retina and connecting to the lateral geniculate nucleus, the superior colliculus, and the pulvinar, has expanded along with the parvocellular pathway, a visual pathway that is involved with color and object recognition. I suggest that expansion of these pathways co-occurred, with the koniocellular pathway being crucially involved (among other tasks) in pre-attentional visual detection of fearful stimuli, including snakes, and the parvocellular pathway being involved (among other tasks) in protecting the brain from increasingly greater metabolic demands to evolve the neural capacity to detect such stimuli quickly.

Interesting...although the connection to snakes ("fearful stimuli, including snakes") isn't exclusive.

[5] A diet that included fruits or nectar (though not to the exclusion of arthropods), which provided sugars as a neuroprotectant, may have been a required preadaptation for the expansion of such metabolically active brains.

Possibly true, no obvious snake influence.

[6] Taxonomic differences in evolutionary exposure to venomous snakes are associated with similar taxonomic differences in rates of evolution in cytochrome oxidase genes and in the metabolic activity of cytochrome oxidase proteins in at least some visual areas in the brains of primates.

Interesting. But the number of primate lineages compared is only three (anthropoids before platyrrhine/catarrhine divergence, and platyrrhines vs. catarrhines after divergence). And the same relation could be explained in terms of brain size alone (if larger brained lineages need greater COX activity).

[7] Raptors that specialize in eating snakes have larger eyes and greater binocularity than more generalized raptors, and provide non-mammalian models for snakes as a selective pressure on primate visual systems.

I wonder why this is -- does it have to do with the motion patterns of snakes compared to other raptor prey (like quick-moving small mammals)? Or the shape and coloration of snakes against likely backgrounds?

[8] These models, along with evidence from paleobiogeography, neuroscience, ecology, behavior, and immunology, suggest that the evolutionary arms race begun by constrictors early in mammalian evolution continued with venomous snakes. Whereas other mammals responded by evolving physiological resistance to snake venoms, anthropoids responded by enhancing their ability to detect snakes visually before the strike.

Unanswered questions

I have to say, I approached this one very skeptically, but after reading it I have a lot of sympathy for the approach. But to start off, I will be very clear about questions that someone might reasonably ask that the paper really doesn't have great answers for:

Are primates really under that much predation from snakes? Venomous snakes in particular? Most primates are pretty big to be the intended prey of venomous snakes, after all…

The paper devotes a section to this question. There have been some observed or suspected instances of snakebite in wild primates, and humans suffer a lot of snakebite -- especially in the tropics. But there just aren't any good numbers, such as relative importance of snakes compared to other predators or mortality risks.

My own feeling about this is that snakes probably are a significant risk to wild primates, but that they are one of many such risks. So the question is whether selection favored effective responses to snakes in particular or instead responses to many predation risks in general.

Distinguishing general from particular is a pretty hard problem -- most of the visual pathways discussed in this paper are useful for detecting all kinds of things, not merely snakes. For example, the paper includes this:

With its emphasis on object recognition, the P pathway would have initially helped those with a diet of fruits, flowers, and nectar to locate foods (and perceive snakes and other salient objects near them). Later, with its emphasis on color, the P pathway would have helped such primates locate foods with the highest levels of sugars (Sumner and Mollon, 1996), thereby more effectively protecting the expanding brain against excitotoxicity.

Or, maybe finding fruits just happened to help evade likely predators including snakes. In other words, there may be a link, but the direction of causation is far from clear.

Can coevolution with snakes really explain large patterns of evolution across the primate order? I mean, sure, maybe living primates have some snake-evasion responses, and better vision would help avoid snakes, but we’re talking about the Paleocene here…

All overarching single-cause hypotheses face this problem: the things they want to explain almost always happened at different times. Here, we have the evolution of larger brains and arboreality early in the Cenozoic (or even the Cretaceous), the evolution of the visual system through the Eocene and Oligocene, the evolution of brain size in different catarrhine lineages during the Oligocene and Miocene, and so on. This paper plays that problem as a strength: snakes plausibly exerted a mortality pressure across all those time intervals, when other hypotheses like nocturnal insect hunting didn't apply to most of them. On the other hand, nocturnal insect hunting doesn't really try to explain later events. A single grandiose over-arching hypothesis may claim a strength that it explains more things, but that is no substitute for testing each of its components. The relationships proposed here are plausible, but few of them admit any ready tests.

So those are some problems for the hypothesis that the paper really doesn't answer well. It might well be that snakes really were such an important mortality risk that ancient primates had adaptations specially to defend against them, and that those adaptations themselves contributed to later primate evolution. But it's not easy to sort out the causes -- maybe those apparent "snake-adaptations" were really initiated for other purposes and happen to be useful for resisting snakes, or maybe they really don't have much to do with snakes one way or the other.

Stuff I liked

But there's lots of clever stuff in this paper, making surprising connections between visual processing, diet, and predation risk. For example, I like this:

The hypothesis that constricting snakes favored larger brain size via greater visual specialization in primates identifies a diet of ripe fruit or nectar as a requirement for, and as a cause of, visual specialization and brain enlargement, but not as the ultimate cause. Recall that high CO [cytochrome oxidase] activity reflects high levels of neuronal metabolic activity and that brains are highly metabolically active tissues. Heightened CO activity is, however, potentially costly in that it can lead to excitotoxicity and neuronal death (Lucas and Newhouse, 1957, Olney, 1969, Olney, 1990, Choi, 1988 and Meldrum and Garthwaite, 1990) without protection against overexposure to glutamate, the main excitatory neurotransmitter in the central nervous system (Orrego and Villanueva, 1993). Glutamate is an amino-acid derivative of glucose (Feldman et al., 1997: 392), and it has widespread effects on the brain. Of particular relevance here is its ability to enhance fear-related learning in the amygdala (Walker and Davis, 2002) and to enhance learning in color discrimination tasks (Popke et al., 2001).
Overexposure to glutamate can be minimized by eating glucose, a sugar found in flowers and ripe fruit (Henneberry, 1989, Romano et al., 1993 and Guyot et al., 2000). If frugivores indeed have larger brains and higher basal metabolic rates than folivores or insectivores of the same body size (Clutton-Brock and Harvey, 1980, Armstrong, 1983, Barton et al., 1995 and Martin, 1996), the difference could be a result of the neuroprotectant property of glucose, obtained from a diet of fruits and flowers.

It seems like fruit-seeking behavior would be adaptive for a primate that maintained high cytochrome oxidase levels, not only globally but in local brain regions (here, the visual system is the focus, but possibly other regions might be implicated). People tend to take for granted that sugar-rich foods would be good for primates, but that is really not obvious -- fruits tend to have low protein levels, for example. So an evolutionary specialization on fruits has costs, and it is important to sort out how and why early primates bore those costs.

The paper has a really good section (called "Frequently asked questions!") that presents strong critiques of a couple of oft-cherished theories of primate evolution. It argues that the "nocturnal visual predation" hypothesis is weak because there is evidence that the key primate characteristics ("orbital convergence, enhanced vision, grasping hands and feet, nails, and large brains") did not evolve together.

And I love this paragraph in the "What about sociality" section:

First, [the social intelligence hypothesis] must explain why sheep (Ovis aries), which are not known for having large brains, are still able to visually recognize and remember as many individuals as there are in a typical baboon group, even after a year of separation (Kendrick and Baldwin, 1987 and Kendrick et al., 2001). In both primates and sheep, the temporal cortex is a major site of facial recognition and memory (Gross et al., 1972, Damasio et al., 1982, Perrett et al., 1992, Kanwisher et al., 1997 and Kendrick et al., 2001).

This is a telling sentence:

Critics of the inclusiveness of this [snake] hypothesis are challenged to explain why it would be easier, or more likely, for primates to evolve large bodies or large, complex groups in response to predators than to modify the mammalian visual system in response to the same threat.

There has been a lot more attention to the evolution of brain size, body size, and group size, and comparatively little to the evolution of the visual system (aside from color). Primates have long life spans compared to other mammals, which means that primates have low average mortality rates as adults. One way to get low mortality is to maximize avoidance of predators. To the extent that large brains facilitate evading predators, they will be correlated with low adult mortality. To the extent that large social groups resist predation, they will be correlated with larger brains.

The interesting relations must be inside the brain -- for instance, are larger neocortex sizes specifically adaptations to group living? Or are they involved with interpreting and acting upon visual signs? Visual signs would include those associated with predators, foods, and other individuals. It's not obvious to me that visual cortex allometry is going to give you a good test of these relations, since adaptation would require interpretation and action upon visual signals, and not merely sensing them.

Anyway, those are some thoughts on the primates vs. snakes paper.

References:

Isbell L. 2006. Snakes as agents of evolutionary change in primate brains. J Hum Evol 51:1-35. DOI link