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Introduction: Evolving neural functions
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THE NEUROSCIENCES, Vol 3, 1991 : pp 3 5 1 -353
Introduction : Evolving neural functions William H. Calvin and Katherine Graubard see a new function emerge from a collection of existing functions, without any immediate change in average anatomical form : Darwin's less well known "functional change in anatomical continuity" . In this issue, we ask what insights such mechanisms provide into evolutionary happenings ; hence our title, "Evolving Neural Functions" . Many scientists believe in evolution, although they have little idea about how it works-other than the notions that mutations drive the process and that these innovations are slowly shaped up for efficiency because of survival of the fittest . Both notions are, alas, somewhat misleading . Evolutionary biologists not only know more of the facts and processes but they have acquired `population thinking', an ability to think in terms of population distributions rather than dichotomies . 2 Instead of saying that men make better airplane pilots than women, a population thinker would say that (were everything else equal) perhaps 60 % of pilots would be men, just as 60 % of television interviewers would be women because of the unequal distribution of verbal abilities-but that the best pilot might nonetheless be a woman and the best talk show host might be a man. A population thinker would picture these distributions in inborn ability being shifted over the years . With each generation, new variants are thrown up, not through mutation but by permutations : all the gene shuffling that takes place during crossing-over as sperm and ova are generated, plus the recombination at fertilization . The surviving distribution is much narrower than that at fertilization : in humans, at least 807o of conceptions are spontaneously aborted ; most of the remaining selection takes place during childhood illnesses and only a fraction of the selection acts on reproductive adults . Boom times allow even rare variants to survive and reproduce ; hard times then narrow the widened distribution and sometimes a new optimum is discovered, as when variants discover an empty niche and fill it . The differential survival is not merely a matter of coping with pathogens, predators, food availability and finding shelter, elements of natural selection that could be called environmental selection ; it is also a matter of quirks in mating systems, usually termed
Evolution does not work logically, or with a long-term perspective, on the design of neural circuits, but rather selects the most successful behavior from generation to generation . Thus there is no reason why the simplest solution to a problem should be the one actually used by the nervous system . As long as both the end result and all the intervening stages work, elegance of design counts for little. The result, in the case of the crayfish escape response, is a confusing mixture of conflicting excitatory and inhibitory pathways . In fact, a common feature of all the examples we have described is that their organization could not have been predicted . It may not be possible to deduce the design of neural circuits by considering the patterns of inputs and outputs, as has been attempted . Such a process of deduction is essentially logical, whereas the evolution of neural circuits is not .
(James P .C . Dumont and R . Meldrum Robertson, 1986) 1 The motto `form follows function' is particularly relevant to brain evolution . Because behavior can be varied without modifying gross anatomy, new functions are usually discovered while using inefficient anatomy, with form subsequently reshaped for efficiency : behavior leads, anatomy follows . But although interest abounds in the evolution of brains, it frequently flounders when the general descends to the specifics of fossils or comparative neuroanatomy . There is, increasingly, a third way to study how brains evolve . In this issue of Seminars in the Neurosciences, we attempt to show what evolutionary insights can be gained from basic neurobiology and ethology . Relationships between structure and function have become a recurrent theme in neurobiology and in studies of animal language-for instance, all of those arguments about whether the vocal tracts of chimpanzee or Neanderthal are capable of human speech . Neural plasticity may allow function to change within a lifetime or, indeed, in days . Across species, we see form being shaped up by function, as might be expected from Darwinian adaptations, and sometimes we can even
University of Washington NJ-15, Seattle, WA 98195, USA ©1991 by W. B . Saunders Company
351
35 2 sexual selection . Male gorillas are twice as large as females for various reasons, 3 most obviously the harem-like mating system ; the predators that they must face do not require such size . Female peacocks seem to make the choice between candidate males based on how long and shiny their feathers are, resulting in a runaway process creating peacocks that are more vulnerable to predators because of their iridescence and cumbersome tails . Higher intellectual abilities could come under environmental selectionorganizing a hunt is the standard example-or, alternatively, be bootstrapped by sexual selection : suppose that females picked mates on the basis of how well they talked, 4 in another runaway process . Some evolution even occurs offline, through the accumulation of unexpressed genes in the genome . With the exception of the X and Y chromosomes in males, humans have two copies of each gene, one of which is passed to each offspring . Some of our genes come in multiple versions, or alleles, so that an offspring may have two versions to choose between ; furthermore, the unexpressed `junk DNA' is full of DNA sequences that look like fragments of known alleles, so that there is the possibility of a new allele being expressed on the rare occasions when the two usual copies are inactivated . A new gene does not usually mean a new feature of the body . Although some genes code for structural proteins, others are regulatory and function only in combination with other genes . The results of changing an allele are often to make only slight changes in a resulting morphology or physiological process . For example, a ratio between several gene products is probably what determines the curvature of a surface-a leaf curves because one sheet of cells grows slower than an underlying one ; a neuron that usually fires in bursts probably is the result of particular ratios of the densities of its channel types, not of a 'bursty channel' gene . We should not expect to find a `big brain' gene but rather a series of changes in developmental rates that result in a head that becomes, relative to body size, somewhat larger than in earlier generations . 5 These changes would be due to a new committee of developmental genes, a far more complicated process than a mere mutation . But evolving new functions is often easier than making such major changes in gross anatomy : as Charles Darwin said, 6 "In considering transitions of organs, it is so important to bear in mind the probability of conversion from one function to another. . . ." The centuries-old motto `nature does
W. H. Calvin and K. Graubard
not take leaps' is only partly true . Anatomy may seldom take leaps but physiology can, because of Darwin's functional change in anatomical continuity . A standard example is that it takes a lot of forelimb feathers to fly even a little ; natural selection for thermal insulation is thought to have shaped feathers up to the threshold for flight . The important point is that a new function, flight, was initially invented with no change in average anatomy . A leap in function occurred and then the average shapes gradually changed as flight efficiency came under natural selection . New uses for old anatomy is probably more important in brain evolution than in any other organ, simply because neurons have a common currency (measured in units called millivolts) with which to compare very different things. We would caution that there is rarely sufficient selection pressure to produce optimal solutions ; the 'good-enough' solutionl ,7 may allow errors and inefficiency to be maintained . One reason why improvements may be slow is the linkage between various traits ; gene combinations may arise that would improve efficiency in one place but decrease it elsewhere . Phylogeny constrains choice ; 8 however handy a fifth leg might be, it is not usually one of the options available (the prehensile tail of the spider monkey being an exception) . Some changes create new problems, yet are under strong enough positive selection pressure to become established ; the lowering of the larynx in the neck may allow humans more versatile vocal utterances than apes but at the price of increased choking and aspiration pneumonia . Epilepsy and some of our mental disorders may well be examples of neural circuit changes with serious side effects . Adaptive organization 9 is "a patchwork of makeshifts pieced together, as it were, from what was available when opportunity knocked, and accepted in the hindsight, not the foresight, of natural selection" . About half of the invited contributions in this issue are 'bottom-up', concerned with how channels evolve (Brehm et al), how neuropils organize (Leise) and how neural circuits vary among species to explore new functionality (Edwards and Palka, Katz) . The other half are concerned with communicative abilities (Brenowitz) and the evolution of higher intellectual functions such as language and plan-ahead consciousness (Falk, Savage-Rumbaugh, Calvin) . But the common theme linking all the articles is the concern with the steps up in functionality that lead to the emergence of more complex behaviors .
Introduction
References 1 . Dumont JPC, Robertson RM (1986) Neuronal circuits : an evolutionary perspective . Science 233 :849-853 2 . Mayr E (1982) The Growth of Biological Thought . Harvard, Cambridge 3 . Cheverud JM, Dow MM, Leutenegger W (1985) The quantitative assessment of phylogenic constraints in comparative analyses : sexual dimorphism in body weight among primates . Evolution 39 :1335-1351 4 . Calvin WH (1992) The unitary hypothesis : a common neural circuitry for novel manipulations, language, plan-ahead, and insight? in Tools, Language, and Intelligence : Evolutionary
3 53
Implications (Gibson K, Ingold T, eds) . Cambridge University Press, to appear 5 . Calvin WH (1990) The Ascent of Mind . Bantam, New York 6 . Darwin C (1859) On the Origin of Species, 1st edn, p 191 . Murray, London 7 . Partridge LD (1982) The good enough calculi of evolving control systems : evolution is not engineering . Am J Physiol 242 :R173-RI77 8 . Huey RB (1987) Phylogeny, history, and the comparative method, in New Directions in Ecological Physiology (Feder ME, Bennett AF, Burggren WW, Huey RB, eds), pp 76-98 . Cambridge University Press, Cambridge 9 . Pittendrigh C, quoted by Calvin WH (1991) The Throwing Madonna, p 88 . Bantam, New York
THE NEUROSCIENCES, Vol 3, 1991 : pp 3 5 1 -353
Introduction : Evolving neural functions William H. Calvin and Katherine Graubard see a new function emerge from a collection of existing functions, without any immediate change in average anatomical form : Darwin's less well known "functional change in anatomical continuity" . In this issue, we ask what insights such mechanisms provide into evolutionary happenings ; hence our title, "Evolving Neural Functions" . Many scientists believe in evolution, although they have little idea about how it works-other than the notions that mutations drive the process and that these innovations are slowly shaped up for efficiency because of survival of the fittest . Both notions are, alas, somewhat misleading . Evolutionary biologists not only know more of the facts and processes but they have acquired `population thinking', an ability to think in terms of population distributions rather than dichotomies . 2 Instead of saying that men make better airplane pilots than women, a population thinker would say that (were everything else equal) perhaps 60 % of pilots would be men, just as 60 % of television interviewers would be women because of the unequal distribution of verbal abilities-but that the best pilot might nonetheless be a woman and the best talk show host might be a man. A population thinker would picture these distributions in inborn ability being shifted over the years . With each generation, new variants are thrown up, not through mutation but by permutations : all the gene shuffling that takes place during crossing-over as sperm and ova are generated, plus the recombination at fertilization . The surviving distribution is much narrower than that at fertilization : in humans, at least 807o of conceptions are spontaneously aborted ; most of the remaining selection takes place during childhood illnesses and only a fraction of the selection acts on reproductive adults . Boom times allow even rare variants to survive and reproduce ; hard times then narrow the widened distribution and sometimes a new optimum is discovered, as when variants discover an empty niche and fill it . The differential survival is not merely a matter of coping with pathogens, predators, food availability and finding shelter, elements of natural selection that could be called environmental selection ; it is also a matter of quirks in mating systems, usually termed
Evolution does not work logically, or with a long-term perspective, on the design of neural circuits, but rather selects the most successful behavior from generation to generation . Thus there is no reason why the simplest solution to a problem should be the one actually used by the nervous system . As long as both the end result and all the intervening stages work, elegance of design counts for little. The result, in the case of the crayfish escape response, is a confusing mixture of conflicting excitatory and inhibitory pathways . In fact, a common feature of all the examples we have described is that their organization could not have been predicted . It may not be possible to deduce the design of neural circuits by considering the patterns of inputs and outputs, as has been attempted . Such a process of deduction is essentially logical, whereas the evolution of neural circuits is not .
(James P .C . Dumont and R . Meldrum Robertson, 1986) 1 The motto `form follows function' is particularly relevant to brain evolution . Because behavior can be varied without modifying gross anatomy, new functions are usually discovered while using inefficient anatomy, with form subsequently reshaped for efficiency : behavior leads, anatomy follows . But although interest abounds in the evolution of brains, it frequently flounders when the general descends to the specifics of fossils or comparative neuroanatomy . There is, increasingly, a third way to study how brains evolve . In this issue of Seminars in the Neurosciences, we attempt to show what evolutionary insights can be gained from basic neurobiology and ethology . Relationships between structure and function have become a recurrent theme in neurobiology and in studies of animal language-for instance, all of those arguments about whether the vocal tracts of chimpanzee or Neanderthal are capable of human speech . Neural plasticity may allow function to change within a lifetime or, indeed, in days . Across species, we see form being shaped up by function, as might be expected from Darwinian adaptations, and sometimes we can even
University of Washington NJ-15, Seattle, WA 98195, USA ©1991 by W. B . Saunders Company
351
35 2 sexual selection . Male gorillas are twice as large as females for various reasons, 3 most obviously the harem-like mating system ; the predators that they must face do not require such size . Female peacocks seem to make the choice between candidate males based on how long and shiny their feathers are, resulting in a runaway process creating peacocks that are more vulnerable to predators because of their iridescence and cumbersome tails . Higher intellectual abilities could come under environmental selectionorganizing a hunt is the standard example-or, alternatively, be bootstrapped by sexual selection : suppose that females picked mates on the basis of how well they talked, 4 in another runaway process . Some evolution even occurs offline, through the accumulation of unexpressed genes in the genome . With the exception of the X and Y chromosomes in males, humans have two copies of each gene, one of which is passed to each offspring . Some of our genes come in multiple versions, or alleles, so that an offspring may have two versions to choose between ; furthermore, the unexpressed `junk DNA' is full of DNA sequences that look like fragments of known alleles, so that there is the possibility of a new allele being expressed on the rare occasions when the two usual copies are inactivated . A new gene does not usually mean a new feature of the body . Although some genes code for structural proteins, others are regulatory and function only in combination with other genes . The results of changing an allele are often to make only slight changes in a resulting morphology or physiological process . For example, a ratio between several gene products is probably what determines the curvature of a surface-a leaf curves because one sheet of cells grows slower than an underlying one ; a neuron that usually fires in bursts probably is the result of particular ratios of the densities of its channel types, not of a 'bursty channel' gene . We should not expect to find a `big brain' gene but rather a series of changes in developmental rates that result in a head that becomes, relative to body size, somewhat larger than in earlier generations . 5 These changes would be due to a new committee of developmental genes, a far more complicated process than a mere mutation . But evolving new functions is often easier than making such major changes in gross anatomy : as Charles Darwin said, 6 "In considering transitions of organs, it is so important to bear in mind the probability of conversion from one function to another. . . ." The centuries-old motto `nature does
W. H. Calvin and K. Graubard
not take leaps' is only partly true . Anatomy may seldom take leaps but physiology can, because of Darwin's functional change in anatomical continuity . A standard example is that it takes a lot of forelimb feathers to fly even a little ; natural selection for thermal insulation is thought to have shaped feathers up to the threshold for flight . The important point is that a new function, flight, was initially invented with no change in average anatomy . A leap in function occurred and then the average shapes gradually changed as flight efficiency came under natural selection . New uses for old anatomy is probably more important in brain evolution than in any other organ, simply because neurons have a common currency (measured in units called millivolts) with which to compare very different things. We would caution that there is rarely sufficient selection pressure to produce optimal solutions ; the 'good-enough' solutionl ,7 may allow errors and inefficiency to be maintained . One reason why improvements may be slow is the linkage between various traits ; gene combinations may arise that would improve efficiency in one place but decrease it elsewhere . Phylogeny constrains choice ; 8 however handy a fifth leg might be, it is not usually one of the options available (the prehensile tail of the spider monkey being an exception) . Some changes create new problems, yet are under strong enough positive selection pressure to become established ; the lowering of the larynx in the neck may allow humans more versatile vocal utterances than apes but at the price of increased choking and aspiration pneumonia . Epilepsy and some of our mental disorders may well be examples of neural circuit changes with serious side effects . Adaptive organization 9 is "a patchwork of makeshifts pieced together, as it were, from what was available when opportunity knocked, and accepted in the hindsight, not the foresight, of natural selection" . About half of the invited contributions in this issue are 'bottom-up', concerned with how channels evolve (Brehm et al), how neuropils organize (Leise) and how neural circuits vary among species to explore new functionality (Edwards and Palka, Katz) . The other half are concerned with communicative abilities (Brenowitz) and the evolution of higher intellectual functions such as language and plan-ahead consciousness (Falk, Savage-Rumbaugh, Calvin) . But the common theme linking all the articles is the concern with the steps up in functionality that lead to the emergence of more complex behaviors .
Introduction
References 1 . Dumont JPC, Robertson RM (1986) Neuronal circuits : an evolutionary perspective . Science 233 :849-853 2 . Mayr E (1982) The Growth of Biological Thought . Harvard, Cambridge 3 . Cheverud JM, Dow MM, Leutenegger W (1985) The quantitative assessment of phylogenic constraints in comparative analyses : sexual dimorphism in body weight among primates . Evolution 39 :1335-1351 4 . Calvin WH (1992) The unitary hypothesis : a common neural circuitry for novel manipulations, language, plan-ahead, and insight? in Tools, Language, and Intelligence : Evolutionary
3 53
Implications (Gibson K, Ingold T, eds) . Cambridge University Press, to appear 5 . Calvin WH (1990) The Ascent of Mind . Bantam, New York 6 . Darwin C (1859) On the Origin of Species, 1st edn, p 191 . Murray, London 7 . Partridge LD (1982) The good enough calculi of evolving control systems : evolution is not engineering . Am J Physiol 242 :R173-RI77 8 . Huey RB (1987) Phylogeny, history, and the comparative method, in New Directions in Ecological Physiology (Feder ME, Bennett AF, Burggren WW, Huey RB, eds), pp 76-98 . Cambridge University Press, Cambridge 9 . Pittendrigh C, quoted by Calvin WH (1991) The Throwing Madonna, p 88 . Bantam, New York