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Evolutionary Neuroscience BEHAVIORAL AND BRAIN SCIENCES (2006) 29,1–36 Printed in the United States of America Pre´cis of Principles of Brain Evolution Georg F. Striedter Department of Neurobiology and Behavior and Center for the Neurobiology of Learning and Memory, University of California at Irvine, Irvine, CA 92697-4550 [email protected] http://www.faculty.uci.edu/profile.cfm?faculty_id¼ 3006 Abstract: Brain evolution is a complex weave of species similarities and differences, bound by diverse rules and principles. This book is a detailed examination of these principles, using data from a wide array of vertebrates but minimizing technical details and terminology. It is written for advanced undergraduates, graduate students, and more senior scientists who already know something about “the brain,” but want a deeper understanding of how diverse brains evolved. The book’s central theme is that evolutionary changes in absolute brain size tend to correlate with many other aspects of brain structure and function, including the proportional size of individual brain regions, their complexity, and their neuronal connections. To explain these correlations, the book delves into rules of brain development and asks how changes in brain structure impact function and behavior. Two chapters focus specifically on how mammal brains diverged from other brains and how Homo sapiens evolved a very large and “special” brain. Keywords: basal ganglia; cladistics; development; hippocampus; homology; lamination; mammal; neocortex; neuromere; parcellation; primate The target book, Principles of Brain Evolution (Striedter Once upon a time, biologists tended to think that evol- 2005), was written partly as an upper-level textbook that ution was guided by a single law of progression that summarizes most of the ideas and much of the data of caused simple organisms to become complex, and evolutionary neuroscience, but it is also an attempt to syn- “lower” species to ascend “the scale,” but that view is no thesize the various ideas about how brains evolve into a longer tenable (Hodos & Campbell 1969). Nor is it sensi- larger framework that is new, at least in aggregate. This ble to argue that all of biology can be explained solely in pre´cis will cover mainly the latter, more synthetic terms of Darwin’s law of natural selection (Rosenberg aspects of the book. In particular, it highlights the 2001), for natural selection has to work with raw materials book’s central argument, which is that brains evolve not that are subject to a variety of other principles or laws, altogether randomly, but in accordance with a set of inter- including what we generally call developmental and/or acting laws or principles. physical constraints (Alberch 1982; Gould & Lewontin 1979). Although this view of biology as being governed by a multitude of laws bothers some philosophers of science (Beatty 1997), it is not really troublesome, for 1. Philosophical framework most complex systems, including those studied by physi- cists, tend to be governed by a variety of laws, forces, and The main aim of evolutionary neuroscience is not just to factors that interact. Therefore, biologists ought not to document the history of brain evolution, but also to whittle down their set of laws, but seek a unitary theory explain it. Reconstructions of what likely happened when that accommodates and unifies a lot of different laws. and where are interesting and important but, ultimately, Because that unifying theory is incomplete, most evol- they are not enough. As Poincare´ (1902) once pointed utionary explanations are just partial explanatory out, scientists must focus not on specific facts but on the “sketches” rather than full-fledged theories. Still, they regularities that tie them together. Only the recognition are a good first step. of those regularities, including so-called laws, enables Within that general framework, the target book’s most scientists to predict future events. This much is widely general purpose is to specify some likely rules, principles, accepted, but the same logic applies also to past events, or laws of brain evolution – and to indicate how they for historical explanations are really predictions in hind- might interact. Regrettably, many of the mentioned prin- sight: given what we know, could we have predicted ciples are vague and the synthesis is incomplete. Hopefully, what actually came to pass? If the answer is affirmative, those imperfections will prompt readers to seek more sup- then we have explained the past. This nomological– porting evidence or to construct alternative hypotheses. deductive approach to history has been discussed exten- Most important, I hope that further work will clarify the sively in the philosophical literature (Hempel 1942), but mechanistic bases of the various brain evolution principles. its application in biology presents some noteworthy pro- Once we know those mechanisms, we will know not only blems. Chief among them is that biological history is gov- why the principles exist, but also why there sometimes erned not by a single law but by a plethora of different laws. are “exceptions to the rule.” Although this goal remains # 2006 Cambridge University Press 0140-525X/06 $12.50 1 Striedter: Pre´cis of Principles of Brain Evolution distant, recent advances in developmental, behavioral, and adding neocortex to an ancestral “smell-brain”) continue computational neuroscience make it possible to envision to hold sway among many non-specialists (MacLean such a mechanistic grounding of brain evolution principles. 1990), even though they have long been disproved (North- Hopefully, that dream will stimulate more neuroscientists cutt 1981). Hopefully, the target book will help dissemi- to engage in evolutionary research. As Hans Spemann nate the major advances (such as neurocladistics) that so (1927), a famous embryologist, once wrote: “We still many evolutionary neuroscientists have labored for (see stand in the presence of riddles, but not without hope of Nieuwenhuys et al. 1998). solving them. And riddles with the hope of solution – An intriguing aspect of the history of evolutionary what more can a man [or woman] of science desire?” neuroscience is that it has been marked by a protracted tug-of-war between those who emphasize species differ- ences in brain organization and those who dwell on simi- 2. History of evolutionary neuroscience larities. One major reason for that tension is that the human mind, when confronted with input as complex Evolutionary neuroscience has pre-evolutionary roots but and multifarious as the data on vertebrate brain organiz- flourished only after Darwin’s (1859) Origin of Species ation, generally seeks order (similarities) amidst confusion; forced increasing numbers of intellectuals to contemplate once order has been detected, it can admit that species “man’s place in nature” (as the title of T. H. Huxley’s book differences exist and then embark on a new round of puts it; see Huxley 1863). Remarkably, Darwin understood seeking similarities. If the human mind indeed works that speciation by natural selection produces family trees, this way, then it is only natural that some scientists, at bushes, or corals (see Fig. 1), rather than linear scales. some points in time, emphasize species similarities while Unfortunately, many of Darwin’s contemporaries contin- others home in on differences. According to the quantum ued to see evolution as unilinear and unfailingly progress- physicist David Bohm (1957), it is precisely this tension ive, with lower species gradually ascending some sort of between similarities and differences, between order and phylogenetic scale (Bowler 1988). This scalar view of evol- disorder, that leads to the discovery of scientific laws and ution has now become extinct among practicing evolution- principles – which is why the target book deals with both ary neuroscientists (see Hodos & Campbell 1969), but it species similarities and differences. The latter are empha- lives on in many other minds. Similarly, many “classic” sized mainly because they have thus far received less notions about how vertebrate brains evolved (e.g., by attention. Figure 1. Darwin’s “Corals of Life.” In one of his early notebooks, Charles Darwin sketched this “coral of life” to illustrate the following thought: “The tree of life should perhaps be called the coral of life, base of branches dead; so that passages cannot be seen – this again offers contradiction to the constant succession of germs in progress” (Notebook B, pp. 25–26, from Barrett 1987). 2 BEHAVIORAL AND BRAIN SCIENCES (2006) 29:1 Striedter: Pre´cis of Principles of Brain Evolution Figure 2. A neuropeptide family. This cladogram depicts a putative phylogeny of peptides in the oxytocin/vasopressin family. The last common ancestor of all vertebrates probably possessed only vasotocin, and extant vertebrates retain this peptide with only minor modifications. Just prior to the origin of jawed vertebrates, the ancestral vasotocin gene probably duplicated and gave rise to a new lineage (dashed lines) that includes a variety of oxytocin-related peptides. Within this more variable lineage, we see both convergent evolution (the evolution of oxytocin in both ratfishes and mammals) and a phylogenetic reversal (the re-evolution of mesotocin in marsupials). Pressed to say which of these peptides is part of the general vertebrate archetype, we can say only that all vertebrates possess at least one member of the oxytocin/vasotocin family. (After Hoyle 1999.) 3. Conservation in vertebrate brains Adult brains can
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