Evolutionary Anthropology 19:37–38 (2010)

BOOK REVIEW

Snakes! The Unified Theory of Everything About Primates? The Fruit, the Tree, and the Serpent: Why We See So Well By Lynne A. Isbell (2009). Cambridge: Harvard University Press. 224 p. $45.00 (cloth). ISBN 978-0-674-03301-6.

Explanations for the enhanced visual system of primates, including stereoscopy, high acuity, and brain enlargement, have been in the making for a century. While traditional views have focused on how these adaptations would have helped early primates obtain food or move in an arboreal environment, Lynne Isbell here expands on an idea first presented in a 2006 paper: predation by snakes provided the selective pressure that lead to the visual system that we have today.1 The strength of Isbell’s hypothesis is how she builds support for the idea from so many angles, drawing from behavior, ecology, paleontology, molecular genetics, biogeography, neuroscience, psychology, and immunology, while throwing in some comparative method for good measure. The book nicely puts these pieces together to explain how constricting snakes could have been the primary force favoring the evolution of enhanced vision in primates and how later exposure to venomous snakes could explain the origins of anthropoids and the differences in the visual systems of Old and New World anthropoids. I came away thinking that Isbell may be on to something, but also that there is too much that doesn’t add up or is not as clear-cut as it is presented. Isbell sets up her hypothesis biogeographically, explaining how primates might well have originated in Indo-Madagascar rather than in North America, Eurasia, or Africa, as is more commonly accepted. There

C 2010 Wiley-Liss, Inc. V

DOI 10.1002/evan.20244 Published online in Wiley InterScience (www.interscience.wiley.com).

they would have faced constricting snakes. She argues that an IndoMadagascar origin is more parsimonious than traditional views since it doesn’t require a rafting event to explain how lemurs got to Madagascar. But is this really more parsimonious? If India and Madagascar split at 80 Ma, but lemurs diverged from lorises and galagos at 60 to 70 Ma, then a rafting event is still needed, either to explain how lorisiformes managed to leave Madagascar or how lemurs later returned. The book then moves on to discuss what primate vision is good for: perceiving depth and breaking camouflage, especially at close range and in the lower visual field. If predation pressure was responsible for these adaptations, then what was preying on Cretaceous primates? Isbell reviews the evidence regarding the origins of the main predators of modern primates, including carnivorous mammals, raptors, and snakes, and concludes that snakes were probably the first and have been the most persistent primate predators. While this chapter is full of interesting information for anyone interested in primate predators, I had some problems with the interpretation of what was there and with what was left out. We’re told in one paragraph that raptors could have been preying on mammals by 80 Ma, which is also the minimum estimate for the age of crown primates, but in the next paragraph Isbell uses numbers that don’t seem to add up to tell us that raptors could not have been predators of early primates. While it’s far from clear that early primates would have been preyed on by raptors, it seems premature to rule it out. Moreover, the chapter discusses what might have been eating Cretaceous primates based only on modern predators; extinct lineages, including the most famous of Cretaceous predators, theropod dinosaurs, get short shrift. Carnivorous mammals from the Cretaceous are mentioned only to be dismissed as necessarily irrelevant to the evolution of mammalian vision; their potential as early primate predators is not men-

tioned. All in all, one could take the evidence to argue that dinosaurs were the first predators of mammals and that carnivorous mammals may well have been preying on primates for as long as snakes have. Despite these objections, I found the idea that constricting snakes favored the enhancement of primate vision to be compelling. But it is in the following chapters, where Isbell argues that later exposure to venomous snakes led to further visual enhancements in anthropoids generally and catarrhines specifically, that, in my view, the hypothesis broke down. It seems true that Malagasy lemurs have never been exposed to venomous snakes, but what about lorises and galagos? These taxa have apparently had the same exposure to venomous snakes as anthropoids. This fact, while acknowledged, is lost in a book that repeatedly refers to prosimian vision in the context of a lack of venomous snakes in Madagascar. Isbell’s hypothesis would be far better supported if lemurs had poorer vision than do African and Asian strepsirhines. Perhaps they do, but this is neither discussed nor predicted. Isbell does very briefly address this question, saying that expansion of the lateral geniculate nucleus (LGN) visual system would not be useful for these nocturnal strepsirhines, just as it’s not useful for other nocturnal mammals, but I found this to be unsatisfying for several reasons. First, in arguing that constrictors were the primary selective force favoring enhanced vision in primates, Isbell points out that the primate LGN is ‘‘clearly more expansive and more complex’’ (p. 47) than that of other mammals. So nocturnal primates apparently found at least some expansion to be useful. Second, the LGN is but one part of the visual system that is claimed to have been modified to make detecting snakes easier. Shouldn’t we expect improved detection abilities in other domains of the visual system? Finally, what about owl monkeys? Shouldn’t we expect anthropoids that have returned to a nocturnal way of life to have lost useless structures as costly as those

BOOK REVIEW

38 Wheeler

in the brain? Perhaps they have, but again, it’s not discussed or predicted. I was also unconvinced that the improved vision of catarrhines relative to that of platyrrhines, with catarrhines having evolved, among other things, routine trichromacy and even more convergent orbits, is due to the greater exposure to venomous snakes that catarrhines have faced in their evolutionary history. For one thing, it’s unlikely that either catarrhines or platyrrhines, with a few exceptions like the tiny callitrichines and small cercopithecoids unfortunate enough to be sympatric with the enormous Gaboon viper, face predation pressure from venomous snakes. Isbell concedes this, but is inconsistent about how important it is, writing at one point that ‘‘venomous snakes would have had to have been major predators of anthropoids’’ (p. 108) to have such an effect on their vision, but later saying that, evolutionarily, this doesn’t matter because ‘‘[w]hether a primate is eaten or just bitten, it is still just as dead’’ (p. 111). But it does matter. Venom isn’t cheap2 and so, as Isbell herself can attest, snakes don’t always bite large primates that approach to within striking distance; the selective pressures for detecting venomous snakes should be far greater for prey species actually targeted by these predators. Second, Isbell is a bit too eager to conclude that platyrrhines radiated in the absence of venomous snakes. Extant platyrrhines are estimated to have begun to diversify between 23 and 17 Ma,3 and Isbell tells us that lancehead vipers began their diversification in South America sometime between 23 and 10 Ma. It is thus well within the realm of possibility that the entire radiation of extant New World monkeys occurred in the presence of vipers. Even if the

radiation did begin in the absence of vipers, New World monkeys have seemingly been exposed to vipers since at least 10 Ma. Shouldn’t we expect widespread convergence with the catarrhine condition? Finally, by adding trichromacy to their visual repertoire, catarrhines would seem to have lost some ability to detect camouflaged objects like snakes. Isbell explains trichromacy in the Old World as necessary for foraging for glucose-rich fruits, a diet required to expand the snake-detecting parts of the brain. Catarrhines then had to compensate for their decreased ability to break camouflage with even more orbital convergence. This strikes me as robbing Peter to pay Paul, but it might be testable: compare the snakedetecting abilities of colorblind and trichromatic individuals in different Old World monkey species that vary in their degree of orbital convergence. In the end, Isbell throws out a few more things about primates that she thinks are explained by snakes: cathemerality can exist only where venomous snakes don’t pose a threat (never mind that some owl monkeys are cathermal); habitual terrestriality is absent in the New World because platyrrhines are poor snake-detectors (never mind that some capuchins are quite terrestrial); and declarative pointing in humans evolved from the need to draw attention to snakes. On the latter point, the argument is that because, as bipeds, our eyes are further from the ground, our ability to locate a snake based just on the gaze of others is reduced, so we uniquely benefit from pointing in this context. However, arboreal primates probably also frequently detect snakes from a couple of meters up or more, so they, too, would presumably benefit if the detector pointed to the snake. But if Isbell is correct, perhaps we should

expect that among peoples at high risk of snake bites, the word for ‘‘snake’’ should be characterized by the kinds of attention-getting, arousal-inducing acoustic features that are typical of the alarm calls of other animals.4 To go full circle, Isbell says in the first pages that she hopes to convince the reader ‘‘that snakes could have been largely responsible for the establishment of primates through their effects on primate vision, and for the differences in vision within primates’’ (p. 7). I am indeed more convinced of the former idea than I expected to be, but not so convinced of the latter. Nevertheless, Isbell has set a high bar for those with competing hypotheses regarding the origins of primate taxa. Although the paper1 alone will give you the gist of the hypothesis, this book is truly one for primatologists of all stripes. Whether you are a primate behavioral ecologist, biogeographer, neuroanatomist, paleontologist, comparative psychologist, or functional morphologist, there is something in this book for you. I suspect that, like me, you will not agree with everything, but you’re sure to learn a lot along the way.

REFERENCES 1 Isbell LA. 2006. Snakes as agents of evolutionary change in primate brains. J Hum Evol 51:1–35. 2 McCue MD. 2006. Cost of producing venom in three North American pitviper species. Copeia 2006:818–825. 3 Hodgson JA, Sterner KN, Matthews LJ, Burrell AS, Jani RA, Raaum RL, Stewart CB, Disotell TR. 2009. Successive radiations, not stasis, in the South American primate fauna. Proc Natl Acad Sci USA 106:5534–5539. 4 Owren MJ, Rendall D. 2001. Sound on the rebound: bringing form and function back to the forefront in understanding nonhuman primate vocal signaling. Evol Anthropol 10:58–71.

Brandon C. Wheeler Department of Anthropology Stony Brook University E-mail: [email protected]